Abstract and Keywords
Important cnidarian contributions to our understanding of nervous system evolution may be found in the arrangement of conducting systems and their interactions. We see multiple, diffuse systems that interact to produce specific behaviors, the compression of conducting systems into compact directional or bidirectional conduction systems, and accumulation of multiple compressed conducting systems into integrating structures like nerve rings. We even see ganglion-like rhopalia that contain bilateral and directional conducting pathways. We now know that this compression and specificity of connections is controlled by conserved sets of genetic commands similar to those found in bilateral animals, and likely in common ancestors. This gradation in centralization is only limited in a directed pathway by the unique radial symmetry of cnidarians. Based on the compression of cnidarian conducting systems into integrating centers (nerve rings and rhopalia), the primary hurdle to cephalization is body symmetry. Medusoid cnidarians possess multiple “brains” connected by conducting systems that, by necessity, are nonpolarized.
Cnidarians are frequently referred to as “nerve net animals” in a way that suggests such diffuse networks of neurons represent the exclusive organization of the nervous systems of representatives of the phylum. This issue will be dealt with later, but since nerve nets are common elements of cnidarian nervous systems, it is worthwhile to begin this chapter with a discussion of nerve net properties.
Foundational investigations on nerve nets were conducted in the late 1800s, and they included both anatomical and physiological data. The former utilized histological staining specific for nervous tissue, including silver stains and vital marking of cells with reduced methylene blue, and eventually including electron microscopy. Physiological work started with cutting experiments, electrical stimulation and recordings of muscular contractions, and later progressed into electrophysiological recordings.
From the combination of morphology and physiology, three important concepts emerged regarding nerve net organization and function. These concepts represent generalizations since there are many modifications and exceptions, but these generalizations have found significant traction in the view of the organization and function of Cnidarian nervous systems. First, is the diffuse nature of the neuronal network. In the most elementary conception of a nerve net, the neurites of bipolar and multipolar neurons are randomly arranged in a two-dimensional lattice in which there is no preferred orientation of the neurites. In this type of system, neurites interact with one another at points where neurites intersect, so spread of electrical information occurs as a wavefront of excitation that sweeps across the two-dimensional network.
Second, nerve nets are considered to be nonpolarized. A wave of excitation can be initiated from any place in the network and will progress away from that site equally well in all directions. This is fully supported through the description of symmetrical synapses using the electron microscope, and with modern electrophysiological recordings of communicating neurons. A major conclusion is that for a specific connection between two neurons, one neuron can be presynaptic in one excitation wave and postsynaptic in another wave.
Third, nerve nets can be through-conducting: Once an impulse is initiated within a nerve net, it can be conducted throughout the entire two-dimensional sheet away from the initiation site. Incrementally and decrementally conducting nerve nets do exist, and they will be considered later; however, the majority of the best described systems in cnidarians do exhibit through-conduction.
Perhaps the most profound and earliest demonstration of these three properties was presented by Romanes (1885), who used marginal strip preparations of the scyphomedusa Aurelia, in which a series of interdigitating cuts provided an extremely tortuous pathway for conduction of muscle activation through the strip (Fig. 1). Despite the nature of the cuts, muscular contraction waves were conducted through the strip in either direction, depending on which end of the strip was initially stimulated. For a contraction wave to navigate these cuts, the conduction system had to be diffuse and through-conducting. Because a contraction wave could be driven in either direction through the network, it also had to be nonpolarized.
Because this basic picture of an idealized nerve net is incorporated in a number of ways in the different Cnidarian groups, usually in modified form, these groups will be treated individually, but in a way that highlights modifications and added complexity to the nerve net concept. Cnidarians include two different body forms: polypoid and medusoid. Sessile and free-swimming lifestyles require quite different muscular and nervous organizations to account for ecological and behavioral peculiarities, so the first groups to be described are those that do not have a medusoid form. This also favors a breakdown of cnidarians based on the class-level organization within the phylum. Even in the three classes that include free-swimming medusoid forms, there are major differences in the neural organization, and specifically in the methods of activation of body musculature.
The Class Anthozoa includes the anemones and corals. Their sessile lifestyle might suggest a behavioral simplicity, considering the nerve net-like organization found in many tissues of Anthozoans. However, behavioral reactions go well beyond reflex reactions and feeding activities, particularly if the time course of the behavioral events is extended into the range of minutes or hours. Pantin (1952) listed behavioral activities that result from subtleties in the relative activation or inhibition of longitudinal and circular musculature in the body wall, oral disc, and tentacles of anemones:
1. Maintenance of shape, which requires activation of muscular activity
2. Enhancement of peristalsis for the purpose of elongation
3. Asymmetrical contractions for bending and swaying movements, the latter initiated when food stimuli are present
4. Use of polarized peristaltic contractions for ingestion of food
5. Antiperistalsis for removal of wastes/indigestibles from the digestive cavity
6. Antiperistaltic contractions used by some for the extrusion of genital products
7. Locomotory activity—such as through muscular waves of the foot
We can add to this list more dramatic behavioral activities of some species that indicate the need for relatively sophisticated neural control of the oral disc, pedal disc, and column musculature:
1. Aiptasia can release the pedal disk from the substrate, and use peristaltic movements to move across the substrate in an oral direction (Portmann, 1926).
2. Stomphia coccinea (the swimming sea anemone) responds to contact by predatory starfish Dermasterias or Hippasteria, and by the nudibranch Aeolidia by rapidly detaching from the substrate and producing a series of alternate flexions of opposite sides of the column to propel the anemone away from the predator (Robson, 1961, 1963; Lawn, 1976).
3. Calliactis parasitica forms a symbiotic relationship with hermit crabs such that prodding by the crab can induce detachment of the anemone’s pedal disk from the substrate, to allow transfer of the anemone to the crab’s shell, or to induce shell-climbing behavior by the anemone (Ross, 1960a, 1970, 1979; Ross & Sutton, 1961a,b). The association provides protection for the hermit crab, specifically from octopus predators (Ross, 1971; Ross & von Boletzky, 1979). In return, the anemone gains motility and possibly food scraps from the hermit crab.
Multiple Conducting Systems
Early electrophysiological work clearly showed three conducting systems were present in anemones (McFarlane, 1969a, 1973). These included the “nerve net,” originally described by Pantin (1935a,b), and two slow systems. The three could be separated by their different conduction properties, thresholds, the location of sites of stimulation sensitivity, and sites for recording. Through additional investigations, various behavioral activities of the anemones were correlated with activity in one or more of the identified conducting systems.
The through-conducting nerve net was shown to be associated with rapid contractions of the tentacles, oral disk (including the sphincter), and the mesenteries (Pantin, 1935a,b; Josephson, 1966; Robson & Josephson, 1969; Pickens, 1969; McFarlane, 1969a, 1973).
The two additional conducting systems were named the Slow System 1 (SS1) and Slow System 2 (SS2), and their recorded electrical activity was correlated with a number of responses in several anemone species (McFarlane, 1969a). For example, preparatory feeding behavior was noted by Parker (1917) that included expansion of the oral disk and expansion of the column. In some species, it also included swaying of the body column. McFarlane (1970) found that applied food extract initiated activity in SS1, and this activity corresponded with oral disk expansion. The expansion was found to be due to relaxation of radial muscle of the oral disk (McFarlane & Lawn, 1972). This suggests that the SS1 system can include, or be initiated by, a chemoreceptive input.
The anemone Calliactis parasitica is found on Buccinum shells that are occupied by a hermit crab of the genus Pagurus. To attach to a shell, Calliactis first uses its tentacles to adhere to the shell, followed by release of the pedal disk. Tentacle contact is maintained while the pedal disk is swung around so it can attach to the shell (Ross, 1960a, 1970, 1979; Ross & Sutton, 1961a,b). Again, a chemosensory cue was suggested for initiation of shell climbing, this time to some “shell factor” (Ross & Sutton, 1961a). Upon tentacle contact with the shell, an increase of SS1 activity was noted, and this increase in activity was associated with pedal disk detachment (McFarlane, 1969b, 1973).
Another species of Calliactis is induced to reattach to a hermit crab’s shell by mechanical stimulation initiated by the crab, which prods the column of the anemone to induce pedal disk release (Ross & Sutton, 1961a,b; Cuttress et al., 1970; Ross, 1970). Similar mechanical stimulation of the column of Calliactis parasitica produced SS1 activity similar to that induced chemically by a Buccinum shell (McFarlane, 1969b, 1973).
Contact between a predatory starfish and the anemone Stomphia coccinea results in a stereotyped behavioral sequence by the anemone, called swimming. Initially, there is a contraction of the tentacles and upper column, followed by extension of the column, relaxation of the upper column and oral disk, detachment of the pedal disk, and alternating longitudinal contractions from opposite sides of the column (Lawn, 1976). The swimming activity can last for 5 minutes. SS1 activity was associated with the initial aspects of the behavioral sequence (Lawn, 1976), and no nerve net or SS2 pulses were recorded during swimming. Furthermore, no impulses have been recorded during the alternate flexions. The entire swimming behavior can be triggered with electrical stimulation that produces SS1 activity with the appropriate temporal patterning found during the starfish-stimulated response.
What about the Slow System 2? Spontaneous contractions of parietal muscles in Calliactis occur in bursts, which correlate with nerve net activity. Once nerve net activity decreases, SS2 activity increases so the nerve net and SS2 produce a rhythm of reciprocal activity (McFarlane, 1972, 1973). The SS2 has been determined to be endodermal, and its activity inhibits endodermal circular and parietal muscles (McFarlane, 1974).
Feeding activity involves all three conducting systems in Calliactis (McFarlane, 1975). Specifically, SS2 activity increases during mouth opening and pharynx protrusion. Similar SS2 activity is induced by food extracts, and duplication of SS2 activity through electrical stimulation produces similar mouth opening and pharynx protrusion.
Circumstantial evidence for a fourth conducting system in Calliactis comes from a delayed SS1 response to column shocks (Jackson & McFarlane, 1976). The threshold for the delayed response is different than the thresholds for the other three systems, and delayed pulses arise from an area other than the stimulation site. This delayed initiation system (DIS) can have a shifting origin, and it is believed to result from pacemaker activity within the system.
Pacemakers and Spontaneous Activity
As mentioned earlier, much of anemone behavior occurs at very slow time scales, and without any observable external stimuli. The description of the DIS and the complexity of behavioral reactions in the context of the slower behavioral phases have led to the conclusion that anemone behavior is a complex interplay between known conducting systems and neuronal pacemakers. For example, evidence suggests that activity in the nerve net is under pacemaker control to produce changes in phases of behavior (McFarlane, 1983). The concept of pacemaker control of behavior is well known from medusae; however, it is also central to the complex behavioral activities of anthozoans where multiple pacemakers are widely distributed throughout the body (McFarlane, 1974).
An important peripheral integrative mechanism was described in anemones by Pantin (1935a,b, 1965) and Ross (1952, 1955), and in medusae by Bullock (1943). The important variables that produce different strengths of muscular contraction are impulse number and frequency, so it is referred to as frequency-dependent facilitation. A facilitation-based muscle sheet can produce contractions with very different contractile properties when neuronal activation has variable temporal characteristics (Ross & Pantin, 1940; Ross, 1952, 1955, 1960b). Furthermore, facilitation in a single muscle group can result when the activating inputs come from different sources. Neuromuscular facilitation is thus an important contributor to behavioral variability since it gives individual conducting systems a direct means for contractile variability. Add the possibility of innervation by more than one conducting system and the possible input from pacemaker systems, and each muscular component of a behavioral act can take variable forms.
Control of Anthozoan Behavior
The complexity of anthozoan behavior belies the apparent structural simplicity of their neural elements. Observed behavioral variability is a result of the interplay between (at least) four known conducting systems and an array of locally conducted responses, superimposed on the system of multiple pacemakers. Add to this the convergence of conducting system inputs to individual muscle systems in the context of neuromuscular facilitation, and even a single muscle sheet can produce quite variable contractions (McFarlane, 1984).
The existence of a centralized nervous system seems unlikely for anthozoans. However, McFarlane (1983, 244) states, “In structural terms actinians lack a centralized nervous system but the proposed network of multipolar cell pacemakers, able to produce various types of patterned output in response to a variety of inputs, shows one of the main functions associated with central nervous systems. It seems reasonable therefore to say that actinians have a diffuse central nervous system.”
Coordination in Colonial Anthozoans
Colonial anthozoans are structurally diverse, yet they have one characteristic in common: Individual anemone-like zooids, as well as specialized zooids, are linked by a common tissue mass. Although individual zooids can show independent behaviors, they are also linked into coordinated behaviors by a colonial nervous system. This colonial coordination was initially investigated by Horridge (1957), including octocorallian and hexacorallian species, where protective zooid retraction could be induced by electrical stimulation of either a single zooid or of the colonial tissue. The pattern of zooid retraction was variable in different species. In some, the colonial system was shown to be through-conducting, and polyp withdrawal was conducted throughout the colony. In other species, the area of zooid retraction was limited regardless of the number and frequency of delivered stimuli (Fig. 2). Yet others were not initially through-conducting, but with repetitive stimulation, the area of zooid retraction increased until the entire colony was involved. To explain this variability, Horridge (1957) proposed that individual neurons in the colonial nerve net were not all active, and variation in the degree of spread depended on the number of active neurons following an individual stimulus. In some colonies, the number of active neurons was relatively low at any one time, so the overall spread of zooid retraction was limited. Horridge postulated that the synaptic connections between neurons were the sites of lability. To explain the increases in the area of zooid retraction with each of a series of stimuli, he raised the possibility of interneural facilitation as being a critical player. In this case, a synapse could fail with the first of a stimulus series, but through facilitation, become conducting following one or more stimuli.
Electrophysiological recordings clearly showed the presence of a colonial nerve net in a variety of anthozoans species (Anderson & Case, 1975; Shelton, 1975a,b,c; Anderson, 1976a,b; Satterlie et al., 1976, 1980; Shelton & McFarlane, 1976; Satterlie & Case, 1979, 1980). Electron microscopical and histological evidence confirmed the presence of colonial nerve networks (Satterlie et al., 1976, 1980; Satterlie & Case, 1978, 1980). Several species in these studies were shown to have two types of colonial impulses: one related to zooid retraction; and a slow one, reminiscent of an anemone slow system but with an unknown function.
The issue of through-conduction versus incremental conduction of colonial responses was revisited with the more precise electrophysiological evaluations. Shelton (1975a,b) found that conduction velocity decreased with distance of conduction within the colonial system, and zooid retraction only occurred after a series of colonial impulses. He suggested that differences in the pattern of colonial responses (through-conducting versus incremental responses) could be due to the decreasing frequency of arriving colonial impulses within a burst, and its effect on neuromuscular facilitation in the zooid musculature responsible for the retraction response. In this case, interneural facilitation was not needed to explain the behavioral differences. However, Anderson (1976a) found that in one species that exhibited incremental zooid withdrawal, the colonial impulses were not through-conducting but were incrementally conducted in a manner similar to the areas of zooid retraction, making an argument for interneural facilitation. Subsequent studies supported both positions: In gorgonians, a through-conducting colonial system produced a limited area of zooid retraction, and the colonial system exhibited decreases in conduction velocities with increasing number of stimuli (Satterlie & Case, 1979). On the other hand, several species of stoloniferan and pennatulacean octocorals exhibited through-conduction of both colonial impulses and zooid retractions, but with an initial increase in conduction velocity with the first few impulses in a series, followed by a subsequent decrease in conduction velocity (Satterlie & Case, 1980; Satterlie et al., 1980). The most likely explanation is that both decreases in conduction velocity in through-conducting colonial systems and interneural facilitation in incrementally conducting colonial systems could play a role in different species.
Through the investigation of colonial anthozoans, we can add two variables to the properties of nerve nets that influence behavioral variability in cnidarians: changes in conduction velocity with repetitive activity in individual conducting systems, and the restricted area of conduction within a nerve net, and the ability of repetitive activity to change that area through interneural facilitation.
Medusoid Cnidarians and Swim Pacemakers—The Fundamental Experiments of Romanes
The “fundamental experiments” of Romanes (1885) on the naked-eyed medusae (hydromedusae) and covered-eyed medusae (scyphomedusae) were designed to locate the pacemakers responsible for initiating contractions of the subumbrellar swim musculature, as well as establishing the concept that swim contractions could be initiated by any one of multiple pacemaker sites around the margin of both types of medusae.
Through cutting experiments on the scyphomedusa Aurelia, the swim pacemakers were found to be restricted to the eight marginal rhopalia—complex sensory/neural structures that each contain an ocellus, a statolith, and other neural and sensory structures. When all eight rhopalia were removed, swimming stopped. Spontaneous contractions were noted when only one or more rhopalia were left intact.
In hydromedusae (several species), removal of the entire margin of the swimming bell was necessary to stop swimming. The pacemakers were determined to be distributed evenly around the margin since leaving only a small piece of margin intact was necessary to observe swim contractions. The location of the intact piece was not critical; it was not localized to any particular sensory structure.
This fundamental difference between hydromedusae and scyphomedusae represents a unique case of convergence since both groups of medusae rely on the contraction of subumbrellar sheets of circular musculature to eject water from the subumbrellar cavity for propulsive forces. Yet the organization of the neuromuscular systems shows significant differences well beyond the locations of pacemakers. In highlighting these differences between the neuromuscular organization of medusae of the Class Scyphozoa and Hydrozoa, the Class Cubozoa will be shown to have a neuromuscular organization that is closely aligned with the scyphozoans.
Medusae of the Class Scyphozoa
Medusoid forms of the Class Scyphozoa attracted much early attention from anatomists and physiologists due to their primary behavioral act: swimming. Rhythmic behavior is attractive to study due to its regularity, and to the modification of that regularity by various types of sensory inputs. Neuromuscular facilitation, as originally described in anthozoans (Pantin, 1935a,b), was demonstrated in the subumbrellar circular muscle of scyphomedusae by Bullock (1943) and by Pantin and Vianna Dias (1952). This sheet of striated muscle cells is innervated by a nerve net composed of relatively large neurons (Schafer, 1878; Horridge, 1954a). The first electrical impulses recorded from this net showed a single impulse preceding each contraction of the musculature (Horridge, 1953, 1954b). Investigation of muscular activity during asymmetrical contractions of the swimming bell revealed evidence for inputs from two distinct nerve nets in the subumbrella (Horridge, 1956a; Fig. 3). The network responsible for the brief swimming contractions (the motor nerve net [MNN], also called the giant fiber nerve net) was found to be through-conducting such that a coordinated contraction of the entire subumbrella produced each swim movement. The second system (diffuse nerve net [DNN]) produced longer, irregular contractions, called slow waves. These slow waves contributed to asymmetrical swim contractions similar to those seen during turning and righting behaviors. Since the DNN appeared to be through-conducting, the role of slow waves in asymmetrical swim contractions was problematical. Horridge (1956a) proposed that significant differences in the conduction velocities of the two conducting systems altered the coordination between swim contractions and slow waves to produce the asymmetrical responses. Furthermore, he showed that the DNN and MNN interacted at the rhopalia, where DNN activity could trigger MNN-activated swim contractions. The general picture of the peripheral nervous system of scyphomedusae is of two parallel conducting systems, one of which (MNN) is the motor system for activation of the swim musculature. The second system performs a sensory function in conducting sensory information to the rhopalia but also a modulatory function for the subumbrellar muscle. In its modulatory role, it can alter the pacemaker activity of the rhopalia and the contractile activity of the swim musculature (Passano, 1965, 1982, 2004).
The identity and function of the MNN have since been confirmed and extended with intracellular recordings, electron microscopy, cell dissociation and culture, and various anatomical techniques, including immunohistochemistry (Patton & Passano, 1972; Passano, 1973, Schwab & Anderson, 1980, 1981; Anderson & Schwab, 1981, 1983, 1984, Grimmelikhuijzen, 1983; Anderson et al., 1992; Carlberg et al., 1995; Moosler et al., 1997; Satterlie & Eichinger, 2014). Most notable, from a physiological perspective, is the nature of the action potentials of scyphozoan neurons—they are similar to those of other animals, suggesting that electrogenesis is not unusual or “primitive” in cnidarians (e.g., Anderson & Greenberg, 2001; Moran et al., 2015).
Symmetrical Synapses and Unpolarized Conduction
Horridge (1954b) used an interesting preparation to perform the first recordings of electrical impulses from a scyphomedusa. He was able to visualize individual neurons within the network of MNN neurons. He then cut away tissue to create a tissue bridge that contained only one of these neurons running across the bridge. He noted that a single large neuron was both necessary and sufficient to conduct a contraction wave across the bridge. More important, excitation could be conducted in either direction through these bridges. This latter observation speaks to the concept of unpolarized conduction within a nerve net and the apparent ability of a single bipolar neuron to engage in meaningful conduction in either direction within the nerve net.
A structural feature of scyphomedusan nerve nets was described to account for this unpolarized conduction: symmetrical neurite-neurite synapses (Horridge & Mackay, 1962; Horridge et al., 1962; Westfall, 1973, 1996; Anderson & Schwab, 1981; Anderson & Grunert, 1988). The synapses have synaptic vesicles on both sides of typical membrane densifications. Similar symmetrical synapses have been described in all four cnidarian classes (Jha & Mackie, 1967; Westfall et al., 1971; Peteya, 1973; Satterlie, 1979; Gray et al., 2009).
Anderson (1985) was able to record from pairs of synaptically connected neurons in the scyphomedusa Cyanea and found that an action potential in one neuron typically induced an action potential in the other neuron with a synaptic delay of around 1 ms (Fig. 4). With repetitive stimulation, the postsynaptic action potential sometimes failed, and in those cases, large amplitude depolarizing synaptic potentials were recorded. Small subthreshold currents induced in one of the neurons did not produce voltage changes in the other neuron, suggesting that the communication was not due to electrical coupling. Furthermore, earlier work confirmed that neurons of this network were neither dye-coupled nor electrically coupled (Anderson & Schwab, 1981). Most important was the observation that the synapses could conduct in either direction—the presynaptic–postsynaptic relationship of the two neurons could be reversed, yet the synaptic delays were equal in either direction (Anderson, 1985).
Scyphozoan Rhopalia Are Simple Ganglia With Sensory and Motor Components
The neuronal organization of the scyphozoan rhopalium has been best studied in Aurelia adult medusae and ephyra (Hyman, 1940; Horridge, 1956b; Yamasu & Yoshida, 1976; Hundgen & Biela, 1982; Nakanishi et al., 2009; Satterlie & Eichinger, 2014). The rhopalium is a tubular structure with a terminal statolith. Proximal to the statolith are three sensory structures: a pigment cup ocellus on the oral side; a pigment spot ocellus on the aboral side; a touch plate consisting of presumed mechanoreceptors, immediately proximal to the pigment spot ocellus. Since the statolith is not organized into a statocyst-like structure, it is believed to operate in conjunction with the touch plate to detect changes in tilt of the medusa (Hundgen & Biela, 1982; Spangenberg et al., 1996). Additional sensory cells are scattered over the rhopalium and surrounding rhopalial niche (Nakanishi et al., 2009; Satterlie & Eichinger, 2014).
Nervous elements of the rhopalium form bilaterally symmetrical networks, some of which leave the rhopalium and connect with the MNN, while others connect with fibers of the DNN (Nakanishi et al., 2009; Garm & Ekstrom, 2010; Fig. 5). The rhopalial nervous system is ectodermal and includes at least seven sensory cell types whose basiepithelial neurites form the identified neuronal elements of the rhopalium. Cell types identified so far are immunoreactive to tyrosinated tubulin, taurine, GLWamide, and FMRFamide (Nakanishi et al., 2009). One network includes neurons that are tubulin and taurine immunoreactive, and form longitudinal fibers within the rhopalial body that also contribute fibers that cross laterally between the longitudinal strands. Fibers from this network exit (or enter) the base of the rhopalium and on each lateral side and connect with the MNN. Another network is made up of neurites from interconnected clusters of FMRFamide-immunoreactive cells. Neurites from this network connect to the DNN via lateral bundles that exit the rhopalial base. GLWamide-immunoreactive cells have neurites that form a network that is confined to the rhopalium.
Some of the sensory cells of the touch plate are taurine-immunoreactive and connect with the tubulin/taurine network of the rhopalium (Nakanishi et al., 2009). Sensory cells of the pigment spot and pigment cup ocelli are FMRFamide-immunoreactive and send processes into the FMRFamide-immunoreactive rhopalial network. Scattered and clustered sensory cells are found in other regions of the rhopalium and include cells immunoreactive to all four antibodies.
The rhopalia also contain the pacemakers for the swim system, so the rhopalia represent complex integration centers that receive information from intrinsic sensory structures and information from extrinsic sensory structures (via the DNN). These inputs are capable of altering the activity of swim pacemakers, which conduct their output via rhopalial pathways to the MNN. Thus, while relatively small in size and simple in organization, the scyphozoan rhopalium performs the primary functions of a ganglion.
Pacemaker Interactions in Medusae
Some of the more common scyphomedusae have eight rhopalia spaced around the margin of the bell. Other species have more, but usually in multiples of four. Lerner et al. (1971) asked if this represents a case of neural redundancy. The interaction between rhopalial pacemakers was initially investigated by Horridge (1959), where he showed that the pacemaker activity of a single, isolated rhopalium was highly variable and irregular. In the intact organism, he proposed that activity in one rhopalium was conducted to the other rhopalia via the MNN and reset the pacemakers in these rhopalia. In this way, the rhopalium with the fastest rhythm would drive swimming until its pacemaker rate dropped below the resetting time of another rhopalium. This would lead to a constant shifting of the “dominant” pacemaker due to their individual irregularity of impulse generation. Inputs from intrinsic and extrinsic sensory systems thus could alter the activity of rhopalial pacemakers (excite or inhibit) so that individual rhopalial pacemakers could be induced to accelerate or to drop out of “contention” for driving swimming. Pacemaker interactions were modeled using linkages between individual artificial pacemakers that had interpulse interval profiles identical to real isolated pacemakers, to determine the effect of linking different numbers of such pacemakers (Horridge, 1959; Lerner et al., 1971; Satterlie & Nolen, 2001 [using cubomedusae]). The models indicated two important consequences of having multiple pacemakers; as pacemaker number increased, the overall swim frequency increased, as did the regularity of the overall output of the pacemaker network (Fig. 6). This translated into a greater regularity of swimming contractions. If one considers the importance of frequency-dependent neuromuscular facilitation in the efficiency of repetitive swim contractions, the benefits of increased average frequency and increased regularity are obvious.
Cubomedusae (which are described later) have only four rhopalia, and two important findings emerged from their pacemaker modeling (Satterlie & Nolen, 2001). First, two types of pacemaker linkages were modeled from observed activity of isolated rhopalia of Carybdea; one with resetting linkages, and one where there were no connections between rhopalia, so they operated independently. The best fit of the real animal data was intermediate between the two types of models, suggesting that in cubomedusae, the pacemaker linkages were semi-independent (resetting at some times but independent at other times). One mechanism for the semi-independence was proposed to involve asymmetric sensory inputs. If inhibitory, the inputs could take a rhopalium out of the pacemaker network for a period of time. Excitatory inputs could produce simultaneous or near simultaneous excitation of more than one rhopalium. Second, the facilitation profiles of the swim system of Carybdea indicated that the average swim frequency of unrestrained animals with all four rhopalia intact was at 80% of the maximal facilitation rate. This permitted a biphasic modulatory potential for the system, where strength of muscle contractions could be increased or decreased from the average facilitation state via sensory inputs to the rhopalial pacemakers. Yet, in the nonmodulated state, the efficiency of the contractile system was still in the 80% facilitation range.
The question of redundancy is thus important since one interpretation of the term suggests an unnecessary duplication. In the case of scyphozoan and cubozoan swim pacemakers, the number of pacemakers will have a significant impact on the overall efficiency of the motor system (via frequency-dependent neuromuscular facilitation) due to the increased average frequency of swim contractions and the greater regularity of those contractions with an increased number of pacemakers. The distribution of multiple rhopalia through the full circumference of the bell margin also allows a more complete monitoring of the environment in these radially symmetrical animals. A large number of rhopalia would allow a more precise detection of asymmetrical sensory stimuli in regulating the activity of the swim system. It is interesting to note that the cubomedusae, which have only four rhopalia, have greatly elaborated sensory structures within the rhopalia (notably the system of six eyes/ocelli in each rhopalium).
Common Features of Scyphomedusae
The organization of the swim musculature is variable in different scyphomedusan species, as exemplified by Aurelia, which have a continuous sheet of circular muscle throughout the subumbrella, and Cyanea, which have a circular disk of circular muscle separated from the margin and with radial strips of muscle that extend toward the margin. Despite these differences, the medusae have two parallel conducting systems that run throughout the subumbrella (MNN and DNN), such that elements of the nerve nets are found in nonmuscular regions between the radial strips of Cyanea. The larger fiber size of the MNN, and its function in producing swim contractions, is common to investigated species. Likewise, the sensory link to the DNN, and its influence on the rhopalial pacemakers, is consistent. The direct modulatory effect of the DNN on the swim musculature has been documented in some species, but it cannot be considered common to all. The integrative role of rhopalia as simple invertebrate ganglia is also consistent, although rhopalial shape can vary from tubular to roundish. Additional elaborations, such as the presence of marginal tentacles, organization of oral arms/tentacles, and the functions of the feeding systems are species-specific and dependent on the unique ecology of each species.
The Scyphozoan Polyp, Strobila, and Ephyra
The polyp of the scyphozoan Aurelia has three major muscle fields: radial muscle of the oral disk, longitudinal muscle of the septa and column, and longitudinal muscle of the tentacles (Chia & Amerongen, 1984). Together they mediate a protective retraction response. The tentacles and oral radial muscle can also produce feeding responses to transfer prey to the mouth (Chapman, 1965). Strobilation of the polyp leads to release of ephyra, each of which has a central disk bearing eight arms, each with a terminal rhopalium. Bending of an arm is used for prey transfer, similar to that of polyp tentacles, and a protective response, called the spasm, involves inward bending of all four arms (Horridge, 1956b).
Electrophysiological recordings demonstrated that the equivalent of swim pacemaker potentials in the ephyra were not present in polyps, suggesting that the swim system (the MNN and rhopalia) develops anew in the ephyra. On the other hand, there is similarity between the feeding reactions (tentacle bending in polyps and arm bending in ephyra) and protective responses (withdrawal of polyp and spasm of ephyra) of the two developmental stages. Schwab (1977) found that the feeding and protective responses were controlled by the equivalent of the DNN. The progression from polyp to ephyra thus involves retention of one conducting system and development of a new one. Similarly, the development from ephyra to medusa involves retention of the MNN and rhopalia, but a repurposing of the DNN to a sensory-based system that modulates pacemaker activity and controls tentacle contractions (Schwab, 1977).
Medusae of the Class Cubozoa
The cubozoans were originally included with the Class Scyphozoa (see Hyman, 1940); however, investigation of the life cycle, and polyp and medusa morphology prompted separation into the separate class, the Cubozoa (Werner et al., 1971, 1976). The separation of the Cubozoa has been supported by molecular phylogenetic analyses (see Collins, 2002, 2009; Marques & Collins, 2004; Bentlage et al., 2009).
Cubomedusae are best known for the structure and optics of their elaborate eyes (Berger, 1898; Martin, 2004; Garm et al., 2007a; O’Connor et al., 2009), their visual control of behavior (Garm et al., 2007b; Petie et al., 2011), the elaborate courtship behavior in some species (Lewis & Long, 2005), and the extreme toxicity of some species (Brinkman & Burnell, 2009). If we revert to the original classification of meduase by Romanes (1885), the cubomedusae are clearly within the group of “covered-eyed medusae,” along with the scyphomedusae. In general, they have four rhopalia that contain the pacemakers for the swim system, with a subumbrellar nerve net serving as the motor network for activating the swim musculature (Conant, 1898; Satterlie, 1979; Satterlie & Spencer, 1979; Laska & Hundgen, 1984; Eichinger & Satterlie, 2014). Unique features of the cubomedusan nervous system will be considered next.
Cubomedusae are fast, active swimmers (Hamner et al., 1995; Shorten et al., 2005), capable of accurate turning behavior (they can make 180o turns in two swim contractions; Garm et al., 2007a). Swimming has been analyzed kinematically (Gladfelter, 1973; Shorten et al., 2005), and turning involves asymmetric contractions of the velarium, a ring of muscular tissue the runs at the margin of the bell that extends perpendicular to the subumbrella.
A subumbrellar nerve net is present that functions like the MNN of scyphomedusae. Neurons of this network produce single action potentials that precede each contraction of the subumbrellar swim musculature (Satterlie & Spencer, 1979; Satterlie, 1979; Fig. 7). Cubomedusae also have a velarium, a shelf-like extension of the subumbrella that extends at right angles to the subumbrella and functions similarly to the velum of hydromedusae—to narrow the bell opening for more efficient water ejection (Gladfelter, 1973). The MNN of cubomedusae innervates circular muscle of the velarium, as well as of the subumbrella, and originates from a nerve ring (see later discussion).
Elaboration of Sensory Structures and the Ganglionic Nature of the Rhopalia
The bilateral organization of cubomedusan rhopalia is best seen in the elaboration of sensory structures, but it also extends to the neural organization (Skogh et al., 2006; Garm & Ekstrom, 2010). Two complex, lensed eyes are centered on the subumbrellar midline, and they are flanked by a symmetrical pair of slit ocelli and by a symmetrical pair of pit ocelli (Fig. 8). A statolith occupies the distal tip of the rhopalium. On the opposite end, the rhopalium is connected to the subumbrella via a narrow stalk.
The complex eyes each have a cellular lens, retina, pigment layer, and a neural layer that connects with the rhopalial neuropil (Berger, 1898; Yamasu & Yoshida, 1976; Laska & Hundgen, 1984; Martin, 2004; O’Connor et al., 2009). The photoreceptors are ciliary and send basal processes into the underlying neural layer (Martin, 2004; Gray et al., 2009). The lensed eyes are of the camera type with fairly poor resolution (Nilsson et al., 2005; Garm et al., 2007a; O’Connor et al., 2009). The photoreceptors are opsin based (Martin, 2004; Coates et al., 2006). Electroretinograms show that the complex eyes have relatively slow responses and have spectral sensitivities that suggest use of a single opsin system (Garm et al., 2007a; O’Connor et al., 2010).
Cubomedusae are able to avoid obstacles, and the avoidance responses are visually guided (Garm et al., 2007b). Avoidance requires spatial resolution that is contrast dependent (Garm et al., 2013). Experiments with tethered Tripedalia showed that visual stimuli initiated turning behavior, including an increase in contraction frequency and an asymmetrical contraction of the velarium (Petie et al., 2011).
Light stimuli alter pacemaker activity; in Tripedalia, a decrease in light intensity triggers an increase in swim frequency with a concomitant increase in contraction regularity, while an increase in light intensity decreases pacemaker frequency and regularity (Garm & Bielecki, 2008). The different eyes/ocelli have distinct effects on pacemaker activity, suggesting a rather sophisticated photic integrative system in each rhopalium (Garm & Mori, 2009). Specifically, the lower lensed eye has an inhibitory influence on pacemaker activity when illuminated, and it excites the pacemakers at light-off. The upper lensed eye and the pit ocelli have the opposite effect. The slit ocelli have variable responses, but overall they are similar to the pit ocelli. It is suggested that the lower lensed eye response optimizes the time the medusae spend in the light shafts of mangrove roots and therefore increases feeding success (Garm & Bielecki, 2008).
The rhopalia have a neuropillar region in the upper and lateral regions, and it is best developed on the side opposite the complex eyes (Satterlie, 2002; Parkefelt et al., 2005; Skogh et al., 2006). In addition to neural layers immediately under the complex eyes and ocelli, several distinct conducting pathways have been found within the neuropil (Martin, 2002, 2004; Satterlie, 2002; Parkefelt et al., 2005; Skogh et al., 2006; Parkefelt & Ekstrom, 2009). Described cell populations include pathways that connect the eyes and ocelli to the pacemaker region, as well as commissural connections, giving a bilateral symmetry to the neural pathways within the rhopalia and suggesting that a significant amount of visual processing occurs within the rhopalia (Parkefelt et al., 2005; Skogh et al., 2006). Compressed networks of neurons are also present, best exemplified by a horseshoe-shaped network partially surrounding the junction of the rhopalial stalk that is immunoreactive to RFamide (and FMRFamide) antibodies (Martin, 2002, 2004; Satterlie, 2002; Plickert & Schneider, 2004; Skogh et al., 2006; Parkefelt & Ekstrom, 2009; Eichinger & Satterlie, 2014). The neuro/sensory development of the cubomedusan rhopalium provides the best and most complex example of a cnidarian ganglion.
As with scyphomedusae, the pacemakers for control of swim contractions are located in the rhopalia. Specifically, they are found in the neuropillar region near the emergence of the rhopalial stalk (Satterlie, 1979). Although the pacemaker cells have not been identified, they are found in the region of the giant neurons described by Skogh et al. (2006). Pacemaker interactions in cubomedusae have been discussed earlier (with scyphomedusae).
Compressed Networks of the Subumbrella: The Nerve Ring and Nerve Tracts
Network compression occurs when the neurons in a nerve net have orientations that are restricted to a single predominant band so that conduction it directional instead of diffuse. The resulting tract is still comprised of a network of neurons rather than long axons as found in the nerves of higher animals. However, the function is much the same.
Cubomedusae have a nerve ring that runs from the proximal attachment of a rhopalial stalk to the two nearby tentacle bases, then to the next two rhopalia, and so on around the bell (Satterlie, 1979; Garm et al., 2007c; Eichinger & Satterlie, 2014; Satterlie, 2014; Fig. 9). The structure of the nerve ring is complex, containing three different cells types including giant neurons (Garm et al., 2007c). In cross section, it was divided into five different areas based on the organization of neurons. Three conduction systems have been described electrophysiologically: the motor system, connected to the rhopalial pacemakers; a bell-wide system for producing protective “crumple” responses; and a photic system conducting light-off responses between rhopalia (Satterlie, 2014). Another system, possibly sensory in nature, is suggested from FMRFamide immunohistochemistry where immunoreactive networks in the rhopalia and rhopalial stalk are interconnected by a restricted network in the nerve ring (Garm et al., 2007c; Eichinger & Satterlie, 2014).
A whole-animal integrative system is thus comprised of the four rhopalia and the interconnecting nerve ring. Based on structural and electrophysiological evidence, that system represents a centralization of function that forms the radially symmetrical equivalent of a central nervous system (Garm et al., 2006; Satterlie, 2011). For example, the integration of photic information is not restricted to a single rhopalium but is spread throughout the rhopalial network via the nerve ring. Similarly, the coordination of motor output from rhopalial pacemakers, and its integrative relationship with rhopalial sensory systems throughout the animal, is enhanced by communication via the nerve ring (Garm et al., 2006; Satterlie, 2011).
Compressed Networks of the Subumbrella: Radial Nerves
Cubomedusae have four perradial bands of smooth muscle that run radially from the margin to the manubrium (Satterlie et al., 2005). These muscle bands are involved in the protective crumple response, which curls the bell margin into the subumbrellar cavity (Satterlie, 2014). A compressed neuronal network overlies these radial muscle bands (Eichinger & Satterlie, 2014). Neurites of the network have a prominently radial orientation so they form the cnidarian equivalent of a nerve. At least two separate conducting systems are suggested to comprise the radial nerves: one is tubulin-immunoreactive, and the other is FMRFamide-immunoreactive. Neurites of both subsystems join the nerve ring at the junction of the nerve ring and the rhopalial stalk. Orally, they are continuous with perradial ridges of the manubrium and appear to be continuous with the tubulin-immunoreactive and FMRFamide-immunoreactive nerve nets of the manubrium (Eichinger & Satterlie, 2014).
Tentacle Conduction Systems
As with the radial nerves, the tentacles and pedalia of cubomedusae have at least two distinct conducting systems (based on immunohistochemistry; Eichinger & Satterlie, 2014). One is the peripheral FMRFamide-immunoreactive network, including putative sensory cells, particularly in the expanded rings of tissue that include batteries of nematocysts. A tubulin-immunoreactive network is deep to the FMRFamide network, possibly associated with the longitudinal musculature, which is located within the mesoglea (Simmons & Satterlie, in preparation). Electrophysiological recordings were not able to distinguish activity in these two conducting systems since the prominent impulses were associated with tentacle withdrawal (Satterlie, 2014). This led to the suggestion that the tubulin-immunoreactive networks of cubomedusae may be motor networks (including the MNN of the swim system), while the FMRFamide-immunoreactive networks may be sensory networks than can have motor or modulatory influences on muscle sheets (like the DNN of scyphomedusae).
At the base of the pedalia, the nerve ring dips down and appears to be in contact with the origin of the tentacular networks. In Tripedalia, a cluster of FMRFamide-immunoreactive cell bodies are found in the pedalial side of this junction, suggesting the presence of a loosely organized integrative centers, and reminiscent of the FMRFamide labeling within the rhopalia (Eichinger & Satterlie, 2014). The tubulin antibody did not label additional cell bodies in this region. This organization is interesting since Thiel (1966) suggested that scyphozoan and cubozoan rhopalia were homologous with the rhopaloids of stauromedusae and the tentacles of polyps. All were considered “tentacle-derived organs.” Developmental genetic evidence further suggested that rhopalia and sensory tentacle bulbs of hydromedusae may be related (Nakanishi et al., 2009). This opens the possibility that the neuron clusters at the base of the cubomedusan tentacles may function as a second set of ganglia that are interconnected to the rhopalia via the nerve ring (as additional components of the centralized nervous system).
The tentacles of cubomedusae are involved in two important behaviors: feeding and protective crumpling. When a tentacle captures prey, the tentacle shortens and the tentacle and pedalium bend inward into the bell opening to transfer the prey to the mouth of the manubrium (Larson, 1976). Chemical, mechanical, or electrical stimulation of a single tentacle produced a burst of tentacular impulses preceding shortening and bending of the recorded tentacle/pedalium (Satterlie, 2014). The response was not conducted to other tentacles. With stronger mechanical or electrical stimuli, all four tentacles undergo a coordinated shortening/bending similar to the single tentacle response, associated with more intense impulse activity in the tentacles. Bending of the tentacles/pedalia into the subumbrellar cavity is associated with contraction of the perradial smooth muscle bands to pull the curl of the margin of the bell inward (Satterlie, 2014). This protective response is called crumpling. Coordination of the tentacles during a crumpling response is via the nerve ring (one of the three identified conducting systems as described earlier).
Exumbrellar Nerve Nets
Cubomedusae, as well as some scyphomedusae, have exumbrellar nematocyst batteries. In both groups, the batteries are interconnected by sparse nerve nets. In cubomedusae, only one net has been found, based on tubulin-immunoreactivity (Eichinger & Satterlie, 2014). In the scyphomedusa Aurelia, two nerve nets are associated with nematocyst batteries, one immunoreactive to tubulin, and the other to FMRFamide (Satterlie & Eichinger, 2014). Electrical correlates of exumbrellar conducting systems have not been recorded.
Medusae of the Class Hydrozoa
The morphological and ecological diversity of hydromedusae is rich, yet basic features of their nervous systems are consistent in a comparative context. The result is an array of unique, species-specific neuronal features superimposed on a groundwork of common properties of the hydromedusan nervous system. Those common properties are discussed next.
Epithelial Conduction: Use of Gap Junctions for Electrical Conduction in Nonnervous Tissue
G. H. Parker (1919) described behavioral activity in some lower animals that involved tissues that did not include neurons. The method of conduction through these nonneural tissues was called “neuroid conduction.” Electrophysiological recordings confirmed that nerve-like impulses could be conducted through epithelia that included neither neurons nor muscle cells (Mackie, 1965; Mackie & Passano, 1968). Now referred to as “epithelial conduction,” Mackie suggested three criteria be considered to document such neuron-free conduction (Mackie, 1965):
• Evidence of meaningful conduction through the tissue
• Recording of electrical potentials underlying the meaningful conduction
• Evidence that neurons are absent in the tissue
Multiple reviews document and describe the role of epithelial conduction systems in the behavior of hydromedusae and siphonophores (Mackie, 1970, 2004a; Spencer, 1974a; Anderson, 1980), and a few examples will be given here.
Many hydromedusae exhibit a protective behavioral response called crumpling, which includes a contraction of tentacles and the manubrium, and an inward curling or bending of the bell margin (Hyman, 1940). Stimulation of the exumbrellar epithelium was able to induce crumpling, and Mackie and Passano (1968) demonstrated that electrical impulses were conducted through this epithelium despite a lack of neurons or muscle cells. The action potentials of epithelial cells were conventional overshooting events (Mackie, 1976, 1978; Spencer, 1978; Josephson & Schwab, 1979). Zooids of colonial siphonophores show crumpling behavior, or modified crumpling, again with the involvement of conducting epithelia (Mackie, 1964, 1965, 1976, 1978).
To fully describe hydromedusan behavior, it is necessary to demonstrate interactions between conducting epithelia and neuronal conducting systems. In the siphonophore Nanomia, epithelial impulses triggered contraction of radial muscles in the velum of the swimming zooids to trigger a reversal in swimming direction, while in Hippopodium, epithelial inputs inhibited swimming (Mackie, 1964). Similar inhibition of swimming was found to involve direct hyperpolarization of the neuronal networks that initiate swim contractions (Mackie, 1975, Spencer, 1981; Mackie et al., 2003). The involvement of neurons in the crumpling response was similarly demonstrated by King and Spencer (1981) and Mackie et al. (2003). Gap junctions were found in conducting epithelia, suggesting a low resistance pathway for intercellular current flow (Josephson & Schwab, 1979). Electrophysiological recordings from other epithelia suggest that epithelial conduction is not limited to the exumbrella of hydromedusae or the equivalent tissues of siphonophores (Mackie, 1976, 1978; Spencer, 1978; Fig. 10).
Myoid Conduction: Conduction Through Muscle Sheets Without the Participation of Neurons
The swim musculature of hydromedusae is comprised of sheets of circular muscle lining the bell, interrupted by radial canals that vary in number in different species. In some hydromedusae, the muscle sheets are aneural, with innervation only occurring at the periphery of the sheets (Keough & Summers, 1976; Singla, 1978a,b; Spencer, 1978, 1979; Chain et al., 1981; Satterlie & Spencer, 1983).
In all species investigated, circular muscle cells within the muscle sheets are interconnected by gap junctions (Mackie & Singla, 1975; Keough & Summers, 1976; Singla, 1978a,b; Spencer, 1979; Satterlie, 1985a, 2008; Satterlie & Spencer, 1983; Kerfoot et al., 1985). In four species (Polyorchis, Aequorea, Aglantha, and Stomotoca), direct electrical coupling between muscle cells has been electrophysiologically demonstrated (Satterlie & Spencer, 1983; Kerfoot et al., 1985; Satterlie, 2008). Furthermore, dye-coupling has been shown in two species, Polyorchis and Aequorea, using Lucifer Yellow or carboxyfluorescein (Satterlie & Spencer, 1983; Satterlie, 2008; Fig. 11).
In some species, notably Aequorea and other leptomedusae, subumbrellar nerve nets are also present within the subumbrellar muscle sheets (Satterlie & Spencer, 1983; Satterlie, 2008). In Aequorea, the circular muscle layer is adjacent to the mesoglea, and that sheet is overlain by a layer of radial epitheliomuscular cells. The circular muscle cells are interconnected by gap junctions, and the radial muscle cells are similarly interconnected (Satterlie, 2008). No connections have been found between cells of the two muscle sheets. Cells in each muscle layer show electrical and dye-coupling. Finally, two distinct nerve nets innervate the musculature, one presumably innervating each of the muscle sheets (Satterlie, 2008). The circular muscle produces swim contractions while the radial muscle is involved in the crumpling response of these oblate medusae.
Fourteen hydromedusan species representing five suborders were investigated using electrophysiological and morphological techniques (Satterlie & Spencer, 1983; Kerfoot et al., 1985). All fourteen had similarly shaped action potentials in the circular swim muscle cells (Fig. 12). The action potentials were broad with a long-lasting shoulder preceding the hyperpolarizing phase. In Aequorea, the action potential duration was related to the duration of the resulting contraction (Satterlie, 1985a). In this way, they resemble the action potentials of vertebrate hearts in producing a squeezing contraction to evacuate a viscous fluid from the fluid pump (heart or jellyfish bell). The difference is functionally important: If the pump is attached, it moves the fluid, whereas if the pump is not attached, it moves through the fluid. In both hearts and hydromedusae, the muscle cells are interconnected by gap junctions and show electrical coupling.
Mackie (1973, 1978) found a pair of oversized neurons in the stem of siphonophores and showed they conducted conventional action potentials that triggered a protective retraction of the zooids, and fast backward swimming of the colony. Since then, several species have been found to have oversized neurons within their nervous systems (see Mackie, 1989). Most notable is a network of large neurons in the inner nerve ring of solitary medusae (Anderson & Mackie, 1977; Singla, 1978a; Spencer & Satterlie, 1980; Spencer, 1981; Satterlie & Spencer, 1983; Satterlie, 1985a,b; Meech & Mackie, 1995; Lin et al., 2001). The neurons that make up the network are all electrically coupled and dye-coupled, and they make up the pacemaker system for swim contractions (Fig. 13). In addition, the oversized neurons provide the primary synaptic output for the swim muscle sheets (Spencer & Satterlie, 1980; Spencer, 1981, 1982; Satterlie & Spencer, 1983; Satterlie, 1985b). This recalls the “fundamental experiments” of Romanes, where only a small piece of the margin, from anywhere on the medusa, was needed to get subumbrellar swim contractions in the Naked-Eyed Medusae (hydromedusae). Each neuron in the network has pacemaker capability, and together they make up a network that controls the timing of contractions of the circularly distributed swim musculature (Spencer, 1981).
The Trachyline medusa Aglantha has a system of giant neurons in addition to the oversized swim pacemaker network. They control the remarkable escape swim that involves a ballistic movement of the medusae due to a rapid, strong contraction of the swim musculature (Donaldson et al., 1980; Roberts & Mackie, 1980). The full response also includes rapid twitch contractions of the tentacles to drive tentacle shortening, and it is triggered by inputs from sensitive mechanoreceptive structures located around the margin of the bell. Appropriate stimulation activates a giant neuron located in the outer nerve ring (the Ring Giant; Roberts & Mackie, 1980), which in turn, synaptically activates eight motor giant neurons, which run radially from the margin toward the bell apex, overlying the radial canals (Meech & Mackie, 1995). The motor giants send neurite branches into the muscle sheets in a circular direction to innervate the swim musculature (Singla, 1978b; Weber et al., 1982). The motor giants represent a neurobiological curiosity since they produce two distinct types of action potentials. Slow calcium spikes are involved in activation of the swim musculature during regular swimming (following input from the pacemaker network), while fast sodium spikes are used to trigger the strong contractions responsible for the ballistic escape swims (Mackie & Meech, 1985; Meech & Mackie, 1995). A similar system of giant neurons controls escape swimming in another trachyline medusa as well (Mills et al., 1985).
Compressed Neuronal Networks of Hydromedusae: The Nerve Rings
Hydromedusae have two compressed networks of neurons that run around the margin of the swimming bell, termed the outer nerve ring and inner nerve ring (Fig. 14). The two are made up of neuronal networks representing multiple conducting systems. As such, they represent a centralized, integrating nervous system. The inner nerve ring includes the electrically coupled network of oversized neurons that serve as the pacemaker and motorneurons for the swim system (Anderson & Mackie, 1977; Singla, 1978a; Spencer & Satterlie, 1980; Spencer, 1981, 1982; Satterlie, & Spencer 1983; Satterlie, 1985a,b; Meech & Mackie, 1995; Lin et al., 2001). In Aglantha, fourteen conducting systems have been identified, eight of which are found in the nerve rings (Mackie, 2004b). Interactions between the conducting systems within the nerve rings can explain the rich behavioral repertoire of Aglantha, which includes swimming, pointing/feeding, protective crumpling, control of tentacle length/contraction, and escape swimming (Fig. 15).
The outer nerve ring contains multiple sensory networks, each of which is also made up of electrically coupled neurons (Spencer & Arkett, 1984; Arkett and Spencer, 1986a,b). Polyorchis has a well-developed shadow response in addition to a graded relationship between light levels and swim frequency (Arkett, 1985). Two networks of electrically coupled neurons, and B and O systems, respond to changes in light intensity and interact with the pacemaker network in the inner nerve ring as well as conducting systems in the tentacles (Spencer & Arkett, 1984; Arkett & Spencer, 1986a,b). Ocelli located at the base of the many tentacles represent one input to the B system, whereas the neurons of the O system are directly photosensitive. Many hydromedusae have ocelli of different levels of complexity (Singla, 1974). In addition, other marginal sensory structures associated with the outer nerve ring include statocysts (Singla, 1975), and mechanoreceptors, such as the tactile combs of Aglantha, which are located at the tentacle bases, and can activate the escape swimming circuitry (Arkett & Mackie, 1988; Mackie, 2004b).
Compressed Neuronal Networks of Hydromedusae: Radial Nerves
Communication between the margin and the manubrium requires radial conduction systems for production of behaviors like crumpling, pointing, and lip flaring (Mackie & Singla, 1975; Spencer, 1975, 1978; Mackie, 2004b). Radial muscle of the subumbrella is either found throughout the subumbrellar muscle sheets, typically overlying the circular swim muscle sheet (Satterlie, 2008), but more often in strands that overlie radial canals of the digestive system (Singla, 1978a; Satterlie, 2002, 2011; Mackie, 2004b). Compressed networks of neurons follow these radial strips of muscle to form radial nerves that allow two-way communication between the manubrium and the margin (Satterlie, 2002, 2011).
Common Features of the Hydrozoan Nervous System
Hydromedusae are extremely diverse in terms of body form, ecology, and behavior, so it is useful to highlight anatomical and physiological features that are common within the group. That allows an analysis of species-specific adaptations that are superimposed on the common features.
One such common feature also sets the hydrozoans apart from the other cnidarians classes: extensive use of gap junctions and electrical coupling between excitable cell types. Excitable epithelia conduct meaningful information from one part of an organism to another, and they interact with the nervous system to contribute to behavioral output (Mackie, 1964, 1965, 1976, 1978; Spencer, 1978; Josephson & Schwab, 1979). Muscle cells within a muscle sheet can conduct electrical impulses without the involvement of neurons (Mackie & Singla, 1975; Keough & Summers, 1976; Singla, 1978a,b; Spencer, 1979; Satterlie & Spencer, 1983; Satterlie, 1985a, 2008; Kerfoot et al., 1985). Finally, networks of electrically coupled neurons are found among the multiple conducting system of the inner nerve ring (Anderson & Mackie, 1977; Singla, 1978a; Spencer & Satterlie, 1980, 1983; Spencer, 1981, 1982; Satterlie & Spencer, 1983; Satterlie, 1985a,b; Meech & Mackie, 1995; Lin et al., 2001), and outer nerve ring of hydromedusae (Spencer & Arkett, 1984; Arkett, 1985; Arkett and Spencer, 1986a,b).
Thus far, convincing evidence of the presence of gap junctions has not been found in three of the four cnidarian classes; Anthozoa, Scyphozoa, and Cubozoa (Mackie et al., 1984; Satterlie, 2002, 2011). However, there is some evidence for intercellular coupling and a connexin-like protein in a colonial anthozoan, Renilla (Germain & Anctil, 1996). Genomic analyses support the separation as up to 19 innexins/pannexins have been found in hydrozoans, while only one has been discovered in an anthozoan, and none have been found in scyphozoans (Moroz & Kohn, 2016). Data on cubozoans are not yet available.
A second common feature is the presence of an oversized network of electrically coupled neurons in the inner nerve ring that function as the pacemaker and primary motorneuron network of the swim system (Anderson & Mackie, 1977; Singla, 1978a; Spencer & Satterlie, 1980, 1983; Spencer, 1981, 1982; Satterlie, 1985a,b, 2002, 2011; Meech & Mackie, 1995; Lin et al., 2001). This network synaptically activates the swim muscle sheets which, as mentioned earlier, are made up of electrically coupled muscle cells.
A third common feature centers on the relationship between the outer nerve ring and the various types of sensory structures located around the margin of the bell. This nerve ring includes multiple conducting systems, at least some of which are made up of electrically coupled neurons. These networks interact with tentacle conducting systems, and with inner nerve ring conducting systems including the swim system (Singla, 1974, 1975; Arkett, 1985; Spencer & Arkett, 1984; Arkett & Spencer, 1986a,b; Arkett & Mackie, 1988; Mackie, 2004b). The types of sensory structures that interact with the outer nerve ring are variable and species-specific.
A potential common feature is the use of radial muscle for pointing/feeding and crumpling responses, although crumping is highly modified in a few species (Mackie & Singla, 1975; Spencer, 1975, 1978; Singla, 1978a; Satterlie, 2002, 2008, 2011; Mackie, 2004b).
Polyps of the Class Hydrozoa
Early work on electrical recording of conducting systems in hydroids confirmed the existence of multiple conducting systems, some of which involved epithelial conduction (Josephson, 1961a,b, 1965, 1967, 1974; Josephson & Mackie, 1965; Josephson & Macklin, 1967, 1969; Josephson & Uhrich, 1969; Josephson & Rushforth, 1973; Mackie, 1968; Passano & McCullough, 1962, 1963, 1964, 1965; Morin & Cooke, 1971a,b; Rushforth, 1971; Rushforth & Burke, 1971; Kass-Simon, 1972; Ball, 1973; Ball & Case, 1973; Spencer, 1974b; deKruijf, 1977). Spontaneous behavioral activity includes rhythmic contractions of the tentacles, hydranth, and body column in various hydroid species (Passano & McCullough, 1963; Josephson & Mackie, 1965; Morin & Cooke, 1971a; Rushforth & Burke, 1971; Josephson & Rushforth, 1973; deKruijf, 1977).
The nervous system of the freshwater Hydra includes a nerve net that extends throughout all parts of the animal (Burnett & Diehl, 1964; Lentz & Barnett, 1965). In addition, gap junctions were initially described between epitheliomuscular cells, between neurons, and between the two cell types in Hydra (Westfall et al., 1971, 1980; Westfall, 1973; Wood, 1977, 1979; Westfall & Kinnamon, 1978). Immunohistochemical labeling suggests that there are six types of neurons that contain different neuropeptides (Grimmelikhuijzen, 1984), and six other types of neurons based on use of other antibodies (Dunne et al., 1985; Yaross et al., 1986; Koizumi et al., 1988, 1992; Hobmayer et al., 1990a,b). While the nervous system is diffuse in most parts of the animal, nerve rings are found between the hypostome and tentacle bases in some hydra species (Matsuno & Kageyama, 1984; Grimmelikhuijzen, 1985; Dunne et al., 1985; Yaross et al., 1986; Koizumi et al., 1992, 2004).
An interesting technique using colchicine treatment resulted in nerve-free Hydra (Campbell et al., 1976). Spontaneous activity is normally observed in untreated animals, but it was absent in the treated animals. Similarly, spontaneous electrical activity in three identified conducting systems (CP system for contraction of the body column; RP system for column elongation; TCP system for tentacle contraction) was absent in the nerve-free animals. Electrical stimulation was able to initiate CP activity and column contraction; however, the impulses occurred at a reduced conduction velocity. This confirms that epithelial conduction exists in Hydra; however, the nervous system was necessary for spontaneous activity and for most coordinated behavioral activities (Campbell et al., 1976).
Ion Channels in Cnidarians
The phylogenetic position of Cnidarians tempts the search for unique features that can be suggested as cnidarian innovations. In this regard, the types and diversity of ion channels found in representatives of three classes (Hydrozoa, Scyphozoa, and Anthozoa) are hardly unique.
In the hydrozoan Aglantha, TTX-resistant sodium currents, calcium currents, and multiple potassium currents have been described in motor giant axons (Meech & Mackie, 1993a,b, 1995). Similar types of currents were found in neurons (Anderson, 1979; Przysiezniak & Spencer, 1992; Jegla et al., 1995; Spafford et al., 1996; Grigoriev et al., 1997) and striated muscle cells (Lin & Spencer, 2001) of another hydrozoan, Polyorchis, and in myoepithelial cells of siphonophores (Inoue et al., 2005). TTX-resistant sodium channels have also been described in the scyphozoan jellyfish Cyanea (Anderson, 1987; Anderson et al., 1993), as has a proton-activated chloride current (Anderson & McKay, 1985). The myoepithelial cells of the anthozoan Calliactis produce action potentials that involve one or two calcium currents and multiple potassium currents (Holman & Anderson, 1991).
Neurotransmission in Cnidarians
Both classical transmitters and neuroactive peptides have been identified from cnidarian tissues (see Leitz, 2001; Grimmelikhuijzen et al., 2002; Kass-Simon & Pierobon, 2007); however, the unequivocal demonstration of their physiological actions remains problematical for most of the candidates that have been identified with morphological or genomic techniques. Some representative examples of investigations designed to identify and study various neuroactive substances are given next.
Evidence for the presence and action of biogenic amines has been found in anthozoans (Anctil et al., 1984, 2002; Hudman & McFarlane, 1995; Gillis & Anctil, 2001), and in hydrozoans (Chung et al., 1989; Chung & Spencer, 1991a,b; Mayorova & Kosevich, 2013). Similarly, the amino acid transmitters glutamate and GABA are active in the modification of chemoreception and control of tentacles of Hydra (Pierobon et al., 2004; Kass-Simon & Scappaticci, 2004). In addition, immunohistochemical labeling in neurons of a scyphozoan (Carlberg et al., 1995) and an anthozoan (Anctil & Minh, 1997) suggests that taurine may play a role in neurotransmission. Both taurine and β-alanine produce synaptic-like responses in isolated chemical synapses of the scyphozoan Cyanea, and both amino acids are present in neurons and are released by depolarization (Anderson & Trapido-Rosenthal, 2009).
A wide variety of neuropeptides have been identified as candidate transmitters/modulators in cnidarian tissues (see Takahashi 2013; Takahashi & Hatta, 2011), and several precursor molecules have sequenced (Gajewski et al., 1996; Moosler et al., 1996; Leviev et al., 1997; Grimmelikhuijzen et al., 2002). RFamides have been extensively studied using immunohistochemical techniques (for example, Grimmelikhuijzen, 1983, 1985, 2002; Grimmelikhuijzen & Spencer, 1984; Mackie et al., 1985; Martin, 1992; Anderson et al., 2004; Fig. 16). Four RFamides have been isolated in Hydra (hydra-RFamide I–IV; Moosler et al., 1996), three in the scyphomedusa Cyanea (Cyanea-RFamide I–III; Moosler et al., 1997), and one RFamide and two RWamides in the anthozoan Calliactis (antho-RFamide, antho-RWamide I and II; McFarlane & Grimmelikhuijzen, 1991). Physiological actions of some of these peptides have been documented (McFarlane, Graff, & Grimmelikhuijzen, 1987; Spencer, 1988; McFarlane et al., 1992). Another family of peptides, the GLWamides, may be ubiquitous to cnidarians (Schmich et al., 1998). Anctil (2009) found four unique GLWamides in the anemone Nematostella and also found evidence for the presence of a peptide in the Gonadotropin-Releasing Hormone family in the anthozoan Renilla (Anctil, 2000).
Physiology of Cnidocyst Discharge
A fundamental type of specialized cell unique to cnidarians is the cnidocyte (nematocyte). Cnidocytes possess various types of projectile threads or barbs, used for enwrapping or penetrating prey, for defensive actions, for aggressive actions, or for adhesion. A notable property of some cnidocytes is the ejection of potent venoms.
Cnidocytes are associated with a variety of sensory and supportive cells, with the multicellular complexes being class-specific (see Rifkin & Endean, 1988; Kass-Simon & Scappaticci, 2002; Thurm et al., 2004; Anderson & Bouchard, 2009). Structural evidence for input and output synapses have been found between cnidocytes and supportive/sensory cells, and gap junctions have been identified in hydrozoans.
The trigger for cnidocyte discharge is complex, and involves a combination of mechanical, chemical, and neural inputs (see Pantin, 1942, for the original work on discharge stimuli). Thurm et al. (2004) suggest that in hydrozoans, there may be as many as four types of sensory cells in cnidocyte batteries, including both chemoreceptors and mechanoreceptors. Chemoreception can include both contact and distance sensing. Mechanical stimulation of sensory cells or cnidocils (ciliary projections from the cnidocytes themselves) is not sufficient to trigger discharge, and various types of receptors have been identified in hydrozoans and anthozoans (reviewed by Anderson & Bouchard, 2009). Putative transmitters and bioactive peptides have been found localized in cnidocytes and associated cells using immunohistochemical techniques (Westfall et al., 2000; Anderson et al., 2004; Kass-Simon & Scappaticci, 2004). These include catecholaminergic, glatamatergic, GABAergic, and neuropeptidergic associations (Fig. 17).
Some nematocysts can be induced to produce action potentials (Anderson & McKay, 1987; Purcell & Anderson, 1995; Brinkmann et al., 1996; Price & Anderson, 2006), and barrages of activity can be triggered by bathing a preparation in an aqueous solution of prey extract (Purcell & Anderson, 1995). In paired recordings from a hydrozoan, cnidocytes within a cluster were electrically coupled and showed similar electrical activity when stimulated (Price & Anderson, 2006). Perhaps the most interesting observation is that cnidocyte discharge is not triggered by current injection sufficient to produce action potentials. Furthermore, not all cnidocytes are capable of producing action potentials (Anderson & McKay, 1987).
Membrane potential is not lost during cnidocyte discharge, which supports the theory that discharge is an exocytotic process (Skaer, 1973; Thurm et al., 2004; Anderson & Bouchard, 2009). Through electrophysiological and molecular cloning methodologies, a number of ion channels have been identified in cnidocyte preparations, including voltage-gated sodium channels, delayed recitifier potassium currents, A-currents, and calcium channels.
The stimulus regime necessary to trigger discharge is not yet fully understood, but cnidocytes do appear to integrate a variety of inputs, including synaptic inputs and direct and indirect chemoreceptive and mechanoreceptive inputs. In addition, chemical and electrical coupling within groups of adjacent or nearby cnidocytes, supportive cells, and sensory cells appears to coordinate the responses of clusters of cnidocytes (see Anderson & Bouchard, 2009).
Cnidarians and the Evolution of Nervous Systems
A great deal of nervous system radiation can be traced to the Cambrian Period, when fossil evidence includes soft-bodied animals, including cnidarians, that show the same complexity as extant species. Some fossils of soft-bodied metazoans date back to the Ediacaran. Through the use of molecular clocks, the origin of metazoans can be pushed back to before the Cyrogenian Period. What about nervous system evolution during these periods?
Molecular clock evidence suggests there were two phases in nervous system evolution (Wray, 2015). The initial phase included relatively simple nervous system structures, with neurons, synapses, and simple effector systems. Sensory structures were simple, as were neuronal processing systems, although rudimentary forms of centralization (including cephalization) were possible. Jekely and colleagues suggest a multicellular nervous system developed to coordinate ciliary swimming in larva-like organisms (Jekely et al., 2011, 2015). Monk and Paulin (2014) suggest the development of spiking neurons coincided with the need for rapid predatory activities. However, the appearance of prey-capture structures like nematocysts and colloblasts preceded the evolution of zooplankton (Budd, 2015). The “skin-brain thesis” suggests the early involvement of excitable epithelia and contractile cells, with the subsequent need for long-distance communication for activation of muscles contributing to the development of neurons (Keijzer et al., 2013).
The second phase involved the formation of elaborate sensory structures and development of more sophisticated neural machinery to integrate the complex sensory information and to activate well-developed effector systems. This second phase is believed to coincide with the later diverse metazoan radiation (Wray, 2015).
Debate continues on whether nervous systems had singular or multiple origins (Moroz, 2009; Budd, 2015). Multicellularity is considered to have evolved only once, based on the presence and composition of collagen and other extracellular matrix proteins (Nielsen, 2012). Similarly, evidence from cell junction proteins argues for a single origin for polarized epithelia and ionic coupling. On the other hand, ion channel and synaptic proteins have been found in unicellular organisms (Emes & Grant, 2012; Burkhardt, 2015).
Moroz (2009) suggests that molecular phylogeny implies that formation of nervous systems occurred at least five to seven times. Furthermore, the lack of neuronal “master genes” suggests multiple independent origins of neurons and synapses (Moroz, 2009; Moroz & Kohn, 2016). Secretory cells may have been the precursors to neurons, and peptides and low molecular weight metabolites are presumed to have been used as interneuronal signals (Moroz & Kohn, 2007).
Interesting relationships are coming from genomic analyses of genes associated with neurogenesis as well as with chemical neurotransmission (Watanabe et al., 2009; Kelava et al., 2015). The formation of neuronal tracts and condensations suggests that genetic programs for axons guidance and neuronal bundling are evolutionarily primitive (Watanabe et al., 2009). Both Hydra and Nematostella have genes required for neurogenesis, neurite targeting, synaptic structure, synaptic transmission, and vesicular transport. In comparing these cnidarians to bilateral animals, there is significant conservation of amino acid sequences and functional domain organizations in various neurogenic programs, as well as for neurogenic transcription factors for neuron differentiation (Watanabe et al., 2009; Kelava et al., 2015).
Together, these data suggest that the common ancestor of cnidarians and bilateral animals may have had a well-developed nervous system with a “genetic toolkit” that included a conserved set of neurogenic, neurodevelopmental, and intercellular signaling genes (Watanabe et al., 2009; Kelava et al., 2015).
Cnidarian Contributions to Our Understanding of Nervous System Evolution
Cnidarians are frequently referred to as “nerve net animals.” An implication of this descriptor is that the nerve net is a defining characteristic of this animal group. However, the question is if this characteristic represents an intermediate step in the evolutionary development of nervous systems found between bilateral animals and some ancestral form. What if the nerve net is simply the most efficient means of synaptically activating muscle fibers that comprise a two-dimensional effector sheet, with the additional requirement that this control can come from any of several potential point-sources of activation? This situation requires a diffuse activation system that can conduct impulses in any direction through the effector sheet—shown as the properties of diffuse, nonpolarized conduction that are characteristic of the “classical” nerve net (Satterlie, 2015a). This would also include a situation in which widespread sensory structures must conduct information to a limited number of integration sites. We certainly see nerve net-like plexuses in higher animals where diffuse, nonpolarized conduction is required to activate two-dimensional effector sheets, particularly those found in the walls of tubular structures, and what if this nerve net organization is just a consequence of the type of radial (or biradial) construction found in cnidarians (Satterlie, 2015a,b)? This would make the nerve net more a nervous system specialization than basal condition.
More important cnidarian contributions to our understanding of nervous system evolution may be found in the arrangement of conducting systems and their interactions. We see multiple, diffuse systems that interact to produce specific behaviors, the compression of conducting systems into compact directional or bidirectional conduction systems, and accumulation of multiple compressed conducting systems into integrating structures like nerve rings. We even see ganglion-like rhopalia that contain bilateral and directional conducting pathways. We now know that this compression and specificity of connections is controlled by conserved sets of genetic commands similar to those found in bilateral animals, and likely in common ancestors. This gradation in centralization is only limited in a directed pathway by the unique radial symmetry of cnidarians. Based on the compression of cnidarian conducting systems into integrating centers (nerve rings and rhopalia), the primary hurdle to cephalization is body symmetry. Medusoid cnidarians possess multiple “brains” connected by conducting systems that, by necessity, are nonpolarized.
Despite this nervous system compression and centralization, the neuronal organization of conducting systems is still net-like. The cells are small and must interact with additional members of the net, typically with connections that are bidirectional. Notable exceptions are the giant neurons found in the specialized conducting systems of several medusoid forms. One possible reason for the dependence on networks of neurons, even when compressed, may represent a property of cnidarian nervous systems that could be considered “primitive.” This is the absence of true axons, where a true axon is considered to have a conducting function that is separate from the communication function that is seen in its axon terminals. In cnidarian neurons, the neurites, even when long, have both conducting and communication functions throughout their length (Satterlie, 2015b). Whether the postsynaptic cells are other neurons within the network, neurons of another conducting system, or effector cells, en passant synapses are the rule, even for giant neurons (Fig. 18). With bilateral symmetry, sensory structures are accumulated in the head end of the organism, and with them we see the condensation of neural structures needed to integrate the sensory information. Cnidarians show this same organization in the association between the accumulation of sensory structures and integrating neural circuitry (as in the nerve rings and rhopalia; Satterlie, 2011). But with cephalization in bilateral animals, the appearance of the ventral nerve cord, and the change in effector organization from widespread, two-dimensional sheets to distinct muscle groups, required (allowed) fast and directional conduction, with a separation between conduction and communication. The full separation is not found in the neurons of many invertebrate groups, but there are examples of neurites in bilateral invertebrates that do show a specialization for conduction only (Satterlie, 2015b).
I thank the American Physiological Society, Elsevier, S. Karger AG, the Royal Society and Springer, and P. A. V. Anderson for permission to use published figures. My work was supported by research grants from the National Science Foundation, by a Guggenheim Fellowship, and by the endowment supporting the Frank Hawkins Kenan Distinguished Professorship at UNCW.
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