Romuald Nargeot and Alexis Bédécarrats
Behaviors of invertebrates can be modified by associative learning in a similar manner to those of vertebrates. Two simple forms of associative learning, Pavlovian and operant conditioning, allow animals to establish a predictive relationship between two events. Here we summarize five decades of studies of behavioral, cellular, and subcellular changes that are induced by these two learning paradigms in different invertebrate animal models. A comparative description of circuitry, neuronal elements, and properties that contribute to these conditioning procedures will be drawn to decipher common and distinguishing features of the learning processes. We will illustrate that similar circuits, synaptic and neuronal membrane plasticity, and similar molecular sites of detection of association are implicated in both forms of conditioning. However, evidence will also suggest that passively responding and endogenous dynamic properties of central networks and/or their constituent neurons might differentially contribute to Pavlovian and operant learning.
Yun Doo Chung and Jeongmi Lee
Hearing in invertebrates has evolved independently as an adaptation to avoid predators or to mediate intraspecific communication. Although many invertebrate groups are able to respond to sound stimuli, insects are the only group in which hearing is widely used. Therefore, we will focus here on the auditory systems of some well-known insect models. Appearance of the ability to perceive sound in insects is presumably a quite recent event in evolution. As a result of independent evolution, diverse types of hearing organs are evolved in insects. Here we will introduce basic features of insect ears and the mechanisms through which sound stimuli are converted into neuronal electric signals. We will also summarize our current understanding of neural processing of auditory information, including tonotopy, sound localization, and pattern recognition.
Reception of chemicals via olfaction and gustation are prerequisites to find, distinguish, and recognize food and mates and to avoid dangers. Several receptor gene superfamilies are employed in arthropod chemosensation: inverse 7-transmembrane (7-TM) gustatory and olfactory receptors (GRs, ORs), 3-TM ionotropic glutamate-related receptors (IRs), receptor-guanylyl cyclases, transient receptor potential ion channels, and epithelial sodium channels. Some of these receptor gene families have ancient origins and expanded in several taxa, producing very large, variant gene families adapted to the respectively relevant odor ligands in species-specific environments. Biochemical and electrophysiological studies in situ as well as molecular genetics found evidence for G-protein-dependent signal transduction cascades for ORs, GRs, and IRs, suggesting that signal amplification is paramount for chemical senses. In contrast, heterologous expression studies argued for primarily ionotropic transduction as a prerequisite to interstimulus intervals in the range of microseconds.
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.
This article reviews the status of research on locomotion in segmented worms. It focuses on three major groups (leeches, earthworms, and nereid polychaetes) that have attracted the most research attention. All three groups show two types of locomotion: crawling (moving over a solid substrate) and swimming (moving through a liquid). The adults of all three groups form a hydroskeleton by controlling the pressure within the segments, and they locomote by controlling the shapes of the individual segments in coordinated spatial and temporal patterns. Many annelid larvae use cilia to move through water. Four aspects of the locomotory patterns are considered: the kinematics (the movement patterns), biomechanics (how muscle contractions produce movement), the neuronal basis of the movement patterns, and efforts to produce robots that move like annelid worms.
Daniel Cattaert and Donald Hine Edwards
This chapter will consider the control of posture and walking in decapod crustaceans (crabs, lobsters, rock lobsters, and crayfish). The walking system of crustaceans is composed of five pairs of appendages, each with seven articulated segments. While crabs sideways walking relies on stereotyped trailing and leading leg movements, forward/backward walking in lobsters and crayfish is achieved by different movements in the different legs, depending on their orientation versus body axis. Largely independent neural networks, localized in each of the 10 hemi-segmental thoracic ganglia, control each leg during locomotion. Each of these networks is modularly organized, with a specific central pattern generator (CPG) controlling each joint. Although coordinating interneurons have been described, inter-joint and inter-leg coordination is largely maintained by sensory feedback. Recently, the key role of proprioceptive signals in motor command processing has been addressed thanks to hybrid system experiments and modelling.
Roy E. Ritzmann and Sasha N. Zill
This article discusses legged locomotion in insects. It describes the basic patterns of coordinated movement both within each leg and among the various legs. The nervous system controls these actions through groups of joint pattern generators coupled through interneurons and interjoint reflexes in a range of insect species. These local control systems within the thoracic ganglia rely on leg proprioceptors that monitor joint movement and cuticular strain interacting with central pattern generation interneurons. The local control systems can change quantitatively and qualitatively as needed to generate turns or more forceful movements. In dealing with substantial obstacles or changes in navigational movements, more profound changes are required. These rely on sensory information processed in the brain that projects to the multimodal sensorimotor neuropils collectively referred to as the central complex. The central complex affects descending commands that alter local control circuits to accomplish appropriate redirected movements.
The complex architecture of the nervous system is the result of a stereotyped pattern of proliferation and migration of neural progenitors in the early embryo, followed by the outgrowth of nerve fibers along rigidly controlled pathways, and the formation of synaptic connections between specific neurons during later stages. Detailed studies of these events in several experimentally amenable model systems indicated that many of the genetic mechanisms involved are highly conserved. This realization, in conjunction with new molecular-genetic techniques, has led to a surge in comparative neurodevelopmental research covering a wide variety of animal phyla over the past two decades. This chapter attempts to provide an overview of the diverse neural architectures that one encounters among invertebrate animals, and the developmental steps shaping these architectures.
The Divergent Evolution of Arthropod Brains: Ground Pattern Organization and Stability Through Geological Time
Nicholas J. Strausfeld
Occasionally, fossils recovered from lower and middle Cambrian sedimentary rocks contain the remains of nervous system. These residues reveal the symmetric arrangements of brain and ganglia that correspond to the ground patterns of brain and ventral ganglia of four major panarthropod clades existing today: Onychophora, Chelicerata, Myriapoda, and Pancrustacea. Comparative neuroanatomy of living species and studies of fossils suggest that highly conserved neuronal arrangements have been retained in these four lineages for more than a half billion years, despite some major transitions of neuronal architectures. This chapter will review recent explorations into the evolutionary history of the arthropod brain, concentrating on the subphylum Pancrustacea, which comprises hexapods and crustaceans, and on the subphylum Chelicerata, which includes horseshoe crabs, scorpions, and spiders. Studies of Pancrustacea illustrate some of the challenges in ascribing homology to centers that appear to have corresponding organization, whereas Chelicerata offers clear examples of both divergent cerebral evolution and convergence.
Vu H. Lam and Joanna C. Chiu
Invertebrates are an incredibly diverse group of animals that come in all shapes and sizes, and live in a wide range of habitats. In order for all these organisms to perform optimally, they need to organize their daily activities and physiology around the perpetuating day-night cycles that exist on Earth. The circadian clock is the endogenous timing system that enables organisms to anticipate daily environmental cycles and governs these roughly 24-hour cellular and overt rhythms. Given its importance to organismal performance and coordination with external environment, it is not surprising that the circadian clock is believed to be ubiquitous in invertebrates. This chapter will discuss the evolution and molecular designs of the invertebrate circadian clocks and describe our current understanding of the circadian clock neuronal network responsible for interpreting external temporal cues and coordinating cellular and physiological rhythms.
Elizabeth C. Cropper, Jian Jing, and Klaudiusz R. Weiss
This review focuses on the neural control of feeding in Aplysia. Its purpose is to highlight distinctive features of the behavior and to describe their neural basis. In a number of mollusks, food is grasped by a radula that protracts, retracts, and hyperretracts. In Aplysia, however, hyperretraction can require afferent activation. Phase-dependent regulation of sensorimotor transmission occurs in this context. Aplysia also open and close the radula, generating egestive as well as ingestive responses. Thus, the feeding network multitasks. It has a modular organization, and behaviors are constructed by combinations of behavior-specific and behavior-independent neurons. When feeding is initially triggered in Aplysia, responses are poorly defined. Motor activity is not properly configured unless responses are repeatedly induced and modulatory neurotransmitters are released from inputs to the central patter generator (CPG). Persistent effects of modulation have interesting consequences for task switching.
Paul McVeigh and Aaron G. Maule
Flatworm nervous systems comprise central and peripheral components that facilitate coordinated and complex behaviors that are modulated by physiological status and sensory input. The absence of a body cavity in flatworms enhances their dependence on neuronal signaling for intercellular communication. Significant advances have been made in our understanding of the neurobiology of flatworms, largely through the growth in genomic/transcriptomic resources and some progress in the development of functional genomics tools. This chapter describes the “state of the art” of flatworm neurobiology with a primary focus on the recent advances made in parasitic flatworms where progress has been driven by the search for new targets for chemotherapeutics.
The main function of brains is to generate adaptive behavior. Far from being the stereotypical, robot-like insect, the fruit fly Drosophila exhibits astounding flexibility and chooses different courses of actions even under identical external circumstances. Due to the power of genetics, we now are beginning to understand the neuronal mechanisms underlying this behavioral flexibility. Interestingly, the evidence from studies of disparate behaviors converges on common organizational principles common to many if not all behaviors, such as modified sensory processing, involvement of biogenic amines in network remodeling, ongoing activity, and modulation by feedback. Seemingly foreseeing these recent insights, the first research fields in Drosophila behavioral neurogenetics reflected this constant negotiation between internal and external demands on the animal as the common mechanism underlying adaptive behavioral choice in Drosophila.
Denise S. Walker, Yee Lian Chew, and William R. Schafer
The nematode Caenorhabditis elegans is among the most intensely studied animals in modern experimental biology. In particular, because of its amenability to classical and molecular genetics, its simple and compact nervous system, and its transparency to optogenetic recording and manipulation, C. elegans has been widely used to investigate how individual gene products act in the context of neuronal circuits to generate behavior. C. elegans is the first and at present the only animal whose neuronal connectome has been characterized at the level of individual neurons and synapses, and the wiring of this connectome shows surprising parallels with the micro- and macro-level structures of larger brains. This chapter reviews our current molecular- and circuit-level understanding of behavior in C. elegans. In particular, we discuss mechanisms underlying the processing of sensory information, the generation of specific motor outputs, and the control of behavioral states.
This article examines the use of invertebrates to investigate the genetic and physiological mechanisms that regulate social behavior. A central goal in behavioral neuroscience is to understand how genes encode behavior and how environmental factors influence the expression of these relevant genes. In pursuit of this goal, many scientists who study behavior use a combined ecological, molecular, genomic, and physiological approach. This article discusses the distinct strengths of an approach, species, or finding in the context of two related but unique social behaviors: aggregation and aggression. It considers the genes that control aggregation and aggression by drawing on insights from C. elegans and Drosophila, respectively. It also describes the neurotransmitters, neuromodulators, and receptors that regulate aggregation and aggression.
While the majority of cellular mRNAs are translated by a cap-dependent mechanism, a subset of mRNAs can use an alternative mode of translation that, instead of cap, relies on discreet RNA elements that help to recruit the ribosome. This mode of translation, termed Internal Ribosome Entry Site (IRES)–dependent translation, is particularly important during conditions of compromised global protein synthesis or for a local, precisely timed translation of specific mRNAs. This latter purpose is of considerable importance in cells of the CNS for their normal function. Recently, the disruption of the IRES-mediated translation has also been linked to pathological processes, suggesting that full understanding and targeting of this peculiar mechanism could be used for therapeutic intervention.
Thomas W. Abrams and Wayne Sossin
During the evolution of synapses, existing molecules were exapted to serve in specific synaptic roles. Recent increased availability of assembled transcriptomes from organisms that evolved before and after the appearance of the earliest synapses provides the opportunity to trace molecular adaptations important for development of fast synaptic transmission. We discuss issues that affect transcriptome assembly and phylogenetic analysis, and which therefore impact this analysis. We use relatively recent transcriptomes of pre-bilaterians to examine the molecular evolution of three types of critical synapse-specific proteins: vesicular transporters, synaptotagmins and ionotropic glutamate receptors. The results emphasize the fundamental difficulties in defining the specific point at which a protein “assumes” a synaptic function. Nevertheless, the analysis informs our understanding of several major evolutionary topics, including the evolution of synaptic vesicles and the identity of the first neurotransmitter used for fast, synchronous transmission. This analysis is also relevant for the current discussion of whether neuronal and synaptic function evolved separately, once in ctenophores and once in cnidarians and the main bilaterian lineage.
Exploiting invertebrates, such as the fruit fly Drosophila or nematode Caenorhabditis, with a modifiable genome seems to be key to answering the fundamental question of the molecular principle of magnetoreception. This review presents the state of knowledge on invertebrate sensitivity to geomagnetic field (GMF) over the last 20 years from a number of viewpoints, with particular emphasis on the behavioral aspect of testing. It shows that experimental approaches are generally specific to the particular research teams, and positive replication at other laboratories is practically nonexistent. The questions surrounding an animal compass are fascinating, but to achieve a level of knowledge of the magnetic sense at least closer to the other senses, a standardized, commercially available, and routinely applicable test on the classic invertebrate model to the natural GMF is still badly needed.
Jiaxing Li and Catherine A. Collins
In the face of acute or chronic axonal damage, neurons and their axons undergo a number of molecular, cellular, and morphological changes. These changes facilitate two types of responses, axonal degeneration and regeneration, both of which are remarkably conserved in both vertebrates and invertebrates. Invertebrate model organisms, including Drosophila and C. elegans, have offered a powerful platform with accessible genetic tools for manipulation and amenable nervous system for visualization. Thus far, several critical components and pathways in axonal degeneration and regeneration have been identified in invertebrate studies, including Sarm and Wallenda/DLK. This article highlights important findings in Drosophila, C. elegans, and other invertebrate injury models that have shed light upon the mechanism in axonal injury response.
Ian A. Meinertzhagen
Despite their often small numbers, the neurons in invertebrate nervous systems can nevertheless constitute many classes, and the nervous systems of little studied or entirely new species still offer significant opportunities for discovery. Circuit analyses and connectomic data are of particular significance, as are the relationships of these to behavior, and the organization of simple larval brains. Functional analyses of synaptic circuits still require knowledge of the neurotransmitter and neurotransmitter receptor for each identified neuron. Synapse complexity ranges widely; undifferentiated pathways in basal species may have unpolarized synapses with presynaptic sites opposite each other, and specialized pathways may have polyadic synapses.