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Neurocognitive Mechanisms of Agrammatism

Abstract and Keywords

This chapter provides a state-of-the-science summary of the neurobiology of agrammatism, an acquired impairment of grammar that may result from stroke or neurodegenerative disease (i.e., primary progressive aphasia). The chapter provides an overview of the language-deficit patterns that characterize agrammatism, such as impaired verb retrieval, verb inflection, verb-argument structure, and production and comprehension of complex sentences. The neurocognitive mechanisms of these deficit patterns are also reviewed, with particular emphasis on recent studies examining the real-time mechanisms of agrammatism and their neural correlates. The picture that emerges is that agrammatism results from impairments of grammatical processing, rather than grammatical knowledge. These deficits largely arise from damage to left hemisphere dorsal language pathways, in particular temporal-parietal and inferior frontal language regions and dorsal white matter tracts.

Keywords: agrammatism, neurodegenerative disease, neurocognitive, verb argument structure, sentence comprehension, sentence production

Introduction

Agrammatism is a language disorder resulting from damage to the (usually) left hemisphere language network. The primary deficit seen in individuals with agrammatism is difficulty producing grammatical sentences. Individuals with agrammatism produce short, grammatically impoverished sentences or sentence fragments, consisting of primarily open class, content words with errors in grammatical morphology, for example, omission and/or substitution of verb inflection (Faroqi-Shah & Thompson, 2003; Saffran, Schwartz, & Marin, 1980; Thompson, Cho, et al., 2012). Consider the following narrative language sample from a 35-year-old male (L.B.S.) with chronic stroke-induced agrammatic aphasia, telling the story of Cinderella:

She’s nice. Dusting (3 sec). Wash (3 sec). The old man (4 sec). Wicked uh sisters uh two three five uh. The horse (5 sec) dog uh bird (3 sec) mouse uh uh is (3 sec) cut (11 sec) dress (2 sec). Be (4 sec) alright. Pumpkin. Pull over uh uh. The uh prince (2 sec). The love uh. We dance (2 sec). Oh no uh noon. How uh get out uh uh? Shoe uh glass shoe (5 sec) found its uh uh. Pulling (3 sec) shoe uh. No ties. Yes. The end.

Linguistic analysis of L.B.S.’s speech using a method developed by Thompson and colleagues (see Thompson, Cho, et al., 2012; Thompson, Shapiro, Li, and Schendel, 1995) revealed a greatly reduced speech rate (i.e., 14 words per minute; mean for healthy age-matched controls = 132.22; standard error of mean [SEM] = 5.22; data from Thompson, Cho, et al., 2012) and utterance length (mean = 2.37 words; mean for healthy controls = 11.11 [SEM = 0.56]). Only 10% of the patient’s sentences were syntactically (p. 797) correct (healthy control mean = 93% [SEM = 1%]), with a complex-to-simple sentence ratio of .10. He also produced more open-class compared to closed-class words (open:closed-class ratio = 2.41; healthy control mean = 0.95 [SEM = 0.03]), with omission of matrix verbs and marked difficulty producing verb inflections (0% correct) (with noun inflection at 100% correct).

These patterns have been borne out in many experimental studies of language production in agrammatic aphasia caused by stroke. In constrained tasks, agrammatic speakers often show ability to produce simple active, canonical sentence structures; however, they show particular difficulty producing sentences with noncanonical word order (Caplan & Hanna, 1998; Cho-Reyes & Thompson, 2012; Faroqi-Shah & Thompson, 2003). Using the Northwestern Assessment of Verbs and Sentences (NAVS; Thompson, 2011; also see Cho-Reyes and Thompson, 2012), which tests production of both canonical forms (i.e., actives, subject-wh questions, and subject-relative structures) and noncanonical forms (passives, object-wh questions, and object-relative constructions) using a sentence production priming task, we (Cho-Reyes & Thompson, 2012) documented this pattern in 35 patients with agrammatic aphasia with mild to moderately severe deficits. Mean production of canonical forms was 72% accurate, compared to a mean of 39% accuracy for noncanonical forms. Studies explicitly examining verb production in agrammatism also show deficits in both verb-naming and sentence-production tasks across languages, including English (Kim & Thompson, 2000; Thompson, Lange, Schneider, & Shapiro, 1997; Thompson, Lukic, King, Mesulam, & Weintraub, 2012; Zingeser & Berndt, 1990), German (De Bleser & Kauschke, 2003), Dutch (Bastiaanse, Hugen, Kos, & van Zonneveld, 2002), Hungarian (Kiss, 2000), Italian (Luzzatti et al., 2002), Russian (Dragoy & Bastiaanse, 2010), Korean (Sung, 2016), and Chinese (Bates, Chen, Tzeng, Li, & Opie, 1991).

Other work has shown that verb inflection is particularly vulnerable in agrammatism. Verb inflections such as subject-verb agreement (e.g., third-person singular present tense -s in English) and tense markings (e.g., English past tense -ed) are missing or incorrectly substituted in agrammatic speech (Arabatzi & Edwards, 2002; Bastiaanse et al., 2011; Burchert, Swoboda-Moll, & Bleser, 2005; Dickey, Milman, & Thompson, 2008; Druks, 2006; Faroqi-Shah & Thompson, 2007; Friedmann & Grodzinsky, 1997; J. Lee, Milman, & Thompson, 2008; Wenzlaff & Clahsen, 2004). In a study testing production of grammatical morphology (using the Northwestern Assessment of Verb Inflection; J. Lee & Thompson, 2017), participants with agrammatism produced fewer correct finite (tensed) verbs (i.e., 53% correct) compared to a group of participants with anomic aphasia (75% correct; Thompson, Meltzer-Asscher, et al., 2013). Similarly, function words such as auxiliaries (e.g., be, have, do) and complementizers (e.g., if, that, whether) are commonly absent (Arabatzi & Edwards, 2002; Friedmann & Grodzinsky, 1997; Milman, Dickey, & Thompson, 2008). Further, nominal functional morphemes such as possessive -s and the definite determiner the can be impaired (Wang, Yoshida, & Thompson, 2014). These patterns have been observed in English, as well as in typologically diverse languages such as German, Hebrew, and Japanese, and across tasks, including spontaneous speech, sentence completion, grammaticality judgment, repetition, and naming (p. 798) (Burchert et al., 2005; Dickey et al., 2008; Friedmann, 2002; Friedmann & Grodzinsky, 1997; Hagiwara, 1995; Milman et al., 2008; Thompson, Meltzer-Asscher, et al., 2013; Wenzlaff & Clahsen, 2004).

Individuals with stroke-induced agrammatic aphasia also evince difficulty comprehending sentences, with particular difficulty understanding complex, noncanonical structures and semantically reversible forms (Caplan, Hildebrandt, & Makris, 1996; Caramazza & Zurif, 1976; Cho-Reyes & Thompson, 2012; Grodzinsky, 2000; Schwartz, Saffran, & Marin, 1980; and many others), where interpretation of “who did what to whom” cannot be derived from semantic or real-world knowledge alone. In one of the first studies of sentence comprehension in aphasia, Caramazza and Zurif (1976) showed that individuals with Broca’s aphasia (and agrammatism) had problems understanding noncanonical, center-embedded sentences such as the girl that the boy is pushing is blond.

The most common cause of agrammatic aphasia is stroke within the distribution of the middle cerebral artery. Associated with Broca’s aphasia, damage to anterior brain tissue (i.e., the left inferior frontal gyrus [IFG], Brodmann’s areas 44 and 45, and adjacent tissue) is common, although research shows that lesions often extend well beyond this region and affect both gray matter and white matter (Cappa, 2012; Catani & Mesulam, 2008; Kertesz, Lesk, & McCabe, 1977; Lukic, Bonakdarpour, den Ouden, Price, & Thompson, 2014; Vanier & Caplan, 1990). Kertesz (1977), using radionucleide to examine lesions in 14 patients presenting with “low fluency associated with relatively well-preserved comprehension” (p. 594), showed that although the common area of infarction involved the IFG (in all patients except one), lesions extended to adjacent frontal as well as temporoparietal tissue. Data from our lab support this pattern. For example, in a recent study including 14 individuals with stroke-induced agrammatism, all participants had lesions in left hemisphere perisylvian regions, including inferior frontal and temporoparietal regions (see Figure 31.1). In addition, recent lesion-symptom mapping studies also implicate both anterior and posterior brain tissue in sentence comprehension and production impairments. For example, in a lesion-symptom mapping study that included 34 patients with stroke-induced aphasia, we (Lukic et al., 2014) found that lesions in anterior (IFG, insula) and posterior perisylvian regions (superior temporal gyrus [STG], angular gyrus [AG], and supramarginal gyrus [SMG]), as well as the arcuate fasciculus (a dorsal white matter tract), significantly predicted agrammatic production deficit patterns (i.e., impaired verb naming, verb-argument structure production, and production of complex sentences).

Agrammatism is also caused by neurodegenerative disease (i.e., primary progressive aphasia [PPA]; see Wilson, Chapter 2 in this volume). One variant of PPA is associated with grammatical deficits (i.e., the agrammatic variant [PPA-G] or nonfluent/agrammatic variant [naPPA]) (Gorno-Tempini et al., 2011; Mesulam, Wieneke, Thompson, Rogalski, & Weintraub, 2012; Thompson & Mack, 2014; Wilson, Galantucci, Tartaglia, & Gorno-Tempini, 2012). We (Mesulam, Thompson, & colleagues; e.g., Mesulam et al., 2009; Mesulam et al., 2012; Thompson, Cho, et al., 2012; Thompson, Meltzer-Asscher, et al., 2013) use the term PPA-G to refer to patients with grammatical (p. 799) impairments, rather than naPPA, since the latter requires one of two core features, either of which is sufficient for classification: (1) agrammatism in language production, and/or (2) motor speech deficits. Importantly, however, not all PPA patients with grammatical impairments present with motor speech difficulty, and patients with “pure” progressive motor speech deficits have been reported who do not evince grammatical impairments (Josephs et al., 2006; Mesulam et al., 2012; Rohrer, Rossor, & Warren, 2010; Wicklund et al., 2014; see Thompson & Mack, 2014, for review). Further, although nonfluent speech production is seen in patients with PPA-G, other variants of PPA also may show nonfluent speech (i.e., logopenic PPA (PPA-L), characterized by impaired word-finding and repetition with intact grammatical abilities), and some evince dissociations between fluency and grammatical ability (Thompson, Cho, et al., 2012). Furthermore, evidence is mixed regarding the degree of overlap between the neural substrates of fluency and grammatical production in PPA (Catani et al., 2013; Gunawardena et al., 2010; Mandelli et al., 2014; Rogalski et al., 2011; Wilson, Henry, et al., 2010).

Neurocognitive Mechanisms of Agrammatism

Figure 31.1. Lesion locations in 14 individuals with agrammatism enrolled in an ongoing study of the neural correlates of language recovery (Thompson lab, in progress). The color bar indicates the number of participants whose lesions overlap at each voxel. Peak areas of overlap (red) include left hemisphere anterior and posterior perisylvian regions, including the inferior frontal gyrus, superior temporal gyrus, and inferior parietal lobule.

Like stroke-induced agrammatism, patients with PPA-G show relatively spared single-word comprehension in the face of impaired grammatical ability in production and complex sentence comprehension impairments (Thompson, Cho, et al., 2012; Thompson & Mack, 2014; Thompson, Meltzer-Asscher, et al., 2013; Wilson et al., 2012). Quantitative analyses of speech samples have typically found more grammatical errors in PPA-G than in healthy age-matched controls or other variants of PPA (e.g., PPA-L, semantic PPA [PPA-S]) (Knibb, Woollams, Hodges, & Patterson, 2009; Thompson, (p. 800) Cho, et al., 2012; Thompson, Meltzer-Asscher, et al., 2013; Wilson, Henry, et al., 2010). Speakers with PPA-G produce fewer syntactically complex utterances (Ash et al., 2009; Gunawardena et al., 2010; Knibb et al., 2009; Wilson, Henry, et al., 2010) than do cognitively healthy controls. Some studies also show a trend toward higher open:closed (O:C) class ratios, with production of fewer verbs compared to nouns (Ash et al., 2009; Thompson, Ballard, Tait, Weintraub, & Mesulam, 1997; Thompson, Cho, et al., 2012; Thompson, Meltzer-Asscher, et al., 2013; Wilson, Henry, et al., 2010) in PPA-G compared to patients with other PPA subtypes. Finally, verb inflection errors (e.g., tense and agreement) in spontaneous language production are prevalent in PPA-G (Thompson, Cho, et al., 2012; Thompson, Meltzer-Asscher, et al., 2013; Wilson, Henry, et al., 2010; also see Graham, Patterson, & Hodges, 2004).

In constrained production tasks, speakers with PPA-G also exhibit grammatical production impairments, particularly for syntactically complex, noncanonical sentences, whereas individuals with PPA-L and PPA-S show relatively unimpaired performance (Cupit et al., 2016; DeLeon et al., 2012; Thompson, Meltzer-Asscher, et al., 2013). We (Thompson, Meltzer-Asscher, et al., 2013) found that while speakers with PPA-G and PPA-L produce canonical sentences (e.g., active sentences, subject wh-questions, and subject-relative clauses) with comparable accuracy, accuracy is significantly lower in PPA-G than in PPA-L for noncanonical forms (e.g., passive sentences, object wh-questions, and object-relative clauses). In addition, verb-production deficits have been quantified in picture-naming tasks. Individuals with PPA-G exhibit more significant impairment in verb (action) naming than in noun (object) naming (Hillis et al., 2006; Hillis, Oh, & Ken, 2004; Hillis, Tuffiash, & Caramazza, 2002; Thompson, Lukic, et al., 2012). However, verb comprehension, like noun comprehension, is largely preserved in PPA-G (Hillis et al., 2006; Thompson, Lukic, et al., 2012). We (Thompson, Meltzer-Asscher, et al., 2013) also found, in a study testing verb inflection using the Northwestern Assessment of Verb Inflection (J. Lee & Thompson, 2017), that PPA-G speakers show greater difficulty producing finite compared to nonfinite verb inflection, suggesting a morphosyntactic locus of verb inflection deficits in this population. Impaired morpho-phonological processing also has been argued to contribute to verb inflection deficits in PPA-G (Wilson, Brandt, et al., 2014). Further, like agrammatism caused by stroke, PPA-G is associated with deficits in comprehension of syntactically complex sentences (Cooke et al., 2003; Gorno-Tempini et al., 2011; Thompson, Meltzer-Asscher, et al., 2013; Wilson, Dronkers, et al., 2010).

Studies measuring cortical thickness in people with PPA-G (compared to cognitively healthy people) show peak atrophy in the left hemisphere IFG, although atrophy is also observed in left hemisphere premotor, dorsolateral prefrontal, and posterior temporoparietal regions in both early and later stages of disease (Mesulam et al., 2009; Mesulam et al., 2012) (see Figure 31.2). Atrophy in the left IFG has been associated with a range of features of agrammatism, including impaired complex sentence comprehension (Amici et al., 2007; Peelle et al., 2008; Wilson et al., 2011) and production (DeLeon et al., 2012; Gunawardena et al., 2010; Rogalski et al., 2011; Wilson et al., 2011; Wilson, Henry, et al., 2010). In addition, agrammatism in PPA is associated with damage to (p. 801) white matter tracts in the left hemisphere (e.g., anterior, posterior and long segments of the arcuate) (Catani et al., 2017; Wilson et al., 2011), as in agrammatism caused by stroke.

Neurocognitive Mechanisms of Agrammatism

Figure 31.2. Sites of cortical atrophy in agrammatic PPA (PPA-G). Orange and yellow areas showed significant atrophy as compared to age-matched controls. Areas of peak atrophy (yellow) in the left hemisphere include the inferior frontal gyrus (IFG), the temporoparietal junction, and premotor and dorsolateral prefrontal regions.

Source: Mesulam et al. (2009).

This chapter is focused on sentence production and comprehension deficits associated with agrammatism, with emphasis on the neurocognitive mechanisms underlying these impairments. Grammatical sentence processing engages lexical as well as morphosyntactic processes. Within the lexical domain, verb processing is particularly germane, since verbs encode syntactic information (i.e., subcategorization frames) as well as verb-argument or event structure (i.e., participant roles entailed within the verb’s representation; see Kemmerer, Chapter 30 in this volume). Thus, verb-argument structure is considered an interface between semantics (e.g., who did what to whom) and syntax (e.g., word order) and is essential for production and comprehension of simple monoclausal sentences, as well as complex syntactic structures, which contain embedded clauses and/or noncanonical argument order (e.g., passive sentences such as The girl was kissed by the boy, in which the Theme argument precedes the Agent). Following many theoretical linguistic models, we assume a “lexicalist” approach in which verb-argument structure guides phrase structure building, which, in turn, mediates sentence processing (Caramazza, 1997; Chomsky, 1981; Horvath & Siloni, 2011; Jackendoff, 1972; Levelt, Roelofs, & Meyer, 1999; Levin & Rappaport, 1986; Reinhart, 2002; Williams, 1981; but see Goldberg, 1995, 2003, for discussion of the “constructivist” approach, which argues that verb-argument structure is strongly tied to semantics). The next section of this chapter discusses verb and verb-argument structure impairments seen in agrammatic aphasia as they relate to sentence comprehension and production abilities. This is followed by discussion of studies examining complex sentence processing in agrammatism. Then, we address neurocognitive mechanisms associated with verb and sentence impairments. Throughout, based on the extant literature, we discuss theories of agrammatism with a focus on impaired thematic integration (i.e., the processes that support the licit combination of a verb’s (p. 802) thematic roles and its constituent arguments to yield the intended meaning of a sentence).

Verb and Verb-Argument Structure Deficit Patterns

Verbs are used to describe different types of events, with different numbers and types of core participants (arguments). For example, some verbs are predominantly used to describe events with one core participant (e.g., swim), whereas others describe events with two (lift) or three (give) core participants. Further, the meanings of verbs select for different sets of thematic roles, encoding the roles that participants play in the event. For example, events described by lift typically encode an Agent and Theme (e.g., John lifted the box), whereas events described by amuse typically encode a Theme and an Experiencer (e.g., The show amused John). On many current accounts, these thematic role labels are a convenient stand-in for a more elaborated lexical-conceptual structure that represents the relationships between event participants (e.g., Levin & Rappaport Hovav, 2005). Verbs also differ with respect to the constraints they place on the syntactic realization of their arguments (subcategorization frames). For example, discover allows both nominal and sentential complements (They discovered the new drug; They discovered that the new drug was effective) whereas produce only allows nominal complements (They produced the new drug). We refer to the semantic and syntactic requirements of verbs as verb-argument structure.

Many studies suggest that the representation of verb meaning and verb-argument structure is intact in agrammatism. The evidence for this view has come from a range of experimental paradigms, including single-word comprehension, cross-modal lexical decision, grammaticality judgments, and structural priming. Agrammatic individuals’ single-verb comprehension is often preserved (but see Miceli, Silveri, Nocentini, & Caramazza, 1988), with no deficits in comprehending verbs with complex argument structures (Kim & Thompson, 2000, 2004; M. Lee & Thompson, 2004; Piñango, 2000; Thompson, Lukic, et al., 2012). Agrammatic speakers also show normal access to subcategorization frames during online sentence processing. As in non-brain-damaged volunteers, reaction times (RTs) are longer for verbs with multiple subcategorization options versus those with only one such option, reflecting exhaustive online access to argument structure representations (Shapiro, Gordon, Hack, & Killackey, 1993; Shapiro & Levine, 1990). Access to information about the relative frequencies of different subcategorization frames also appears to be intact (DeDe, 2013a, 2013b). Individuals with agrammatism also evince relatively preserved ability to distinguish sentences with correct argument structure (e.g., The boy is carrying the girl; The dog is barking) from argument structure violations, such as argument omission (e.g., *The boy is carrying) and argument insertion (e.g., * The dog is barking the girl) (Grodzinsky & Finkel, 1998; Kim (p. 803) & Thompson, 2000, 2004; though see Kielar, Meltzer-Asscher, & Thompson, 2012), indicating intact access to sentence-level argument-structure representations. They also show intact priming of the order of thematic roles in sentence production, supporting the view that argument structure representations are intact (Cho-Reyes, Mack, & Thompson, 2016).

However, despite apparently intact argument structure representations, some aspects of the online processing of verbs and verb-argument structure are impaired. Individuals with agrammatism caused by stroke have demonstrated impaired online responses to argument-structure violations (e.g., *John sneezed the doctor), including abnormal event-related potential (ERP; see Leckey & Federmeier, Chapter 3 in this volume) signals (Kielar et al., 2012), and reaction times (Myers & Blumstein, 2005). In contrast with healthy adults, they also show deficits in using the verb’s selectional restrictions (e.g., that eat requires an edible direct object, but move does not) to predict and integrate arguments (Mack, Ji, & Thompson, 2013; cf. Dickey & Warren, 2015, who report impaired online verb-argument integration in a group of four individuals with stroke-induced aphasia, two of whom have Broca’s aphasia). In PPA-G, two studies have revealed impaired online processing of verb-argument structure violations, one using ERP (Barbieri et al., 2016) and one using reaction-time measures (Peelle, Cooke, Moore, Vesely, & Grossman, 2007); however, one study found intact online processing of these violations (Price & Grossman, 2005). Further, our preliminary research shows impaired verb-argument prediction in listeners with PPA-G (Mack, Mesulam, & Thompson, 2017). Overall, the picture that emerges is that agrammatic individuals’ representation of verb meaning and verb-argument structure seems to be spared, but thematic (i.e., verb-argument) integration is impaired, as shown by abnormal online responses to violations and impaired prediction.

Verb retrieval and verb-argument structure processing is, however, impaired in production. Speakers with agrammatism caused by stroke and PPA produce frequent verb-argument structure errors in structured tasks and in spontaneous language production (Thompson, Ballard, et al., 1997; Thompson, Cho, et al., 2012; Thompson, Lange, et al., 1997; Thompson et al., 1995). Several studies have shown that argument structure complexity affects verb retrieval and sentence-production accuracy. Notably, the literature on argument-structure complexity in agrammatism encompasses typologically diverse languages including English (Thompson, 2003), Dutch (Bastiaanse & van Zonneveld, 2005), German (De Bleser & Kauschke, 2003), Greek (Stavrakaki, Alexiadou, Kambanaros, Bostantjopolou, & Katsarou, 2011), Hungarian (Kiss, 2000), Italian (Luzzatti et al., 2002), Russian (Dragoy & Bastiaanse, 2010), and Korean (Sung, 2016).

Argument number is one relevant factor that shapes verb production in agrammatism; for example, two- and three-argument verbs (e.g., lift, give) are named less accurately than one-argument verbs (e.g., swim) (Kim & Thompson, 2000, 2004; Kiss, 2000; Luzzatti et al., 2002; Sung, 2016; Thompson, Lange, et al., 1997; Thompson, Lukic, et al., 2012). These effects are shown in both stroke-induced agrammatism and PPA-G (Thompson, Lukic, et al., 2012). The number of arguments selected by the verb (p. 804) also affects both structured sentence production tasks and narrative production: two- and three-argument sentences are produced less frequently and/or accurately than in unimpaired speakers (Bastiaanse & Jonkers, 1998; De Bleser & Kauschke, 2003; Dragoy & Bastiaanse, 2010; Thompson, Lange, et al., 1997). Related to this, a recent study examined the verb’s number of subcategorization frames (i.e., complement types) as a potential factor affecting aphasic sentence production in narratives (Malyutina, Richardson, & den Ouden, 2016). In this study, speakers with Broca’s aphasia produced verbs with fewer arguments and less diverse subcategorization frames, consistent with the idea that thematic integration is impaired in production.

In addition, agrammatism is associated with deficits in producing unaccusative verbs, that is, one-argument verbs in which the grammatical subject is assigned the Theme role (e.g., The man fell; first described by Perlmutter, 1978), in contrast with unergative verbs, which have an Agent subject (e.g., The man swam). These deficits have been observed in verb naming (Luzzatti et al., 2002; Sung, 2016; Thompson, 2003) and in sentence production (Bastiaanse & van Zonneveld, 2005; Dragoy & Bastiaanse, 2010; Kegl, 1995; M. Lee & Thompson, 2004; Stavrakaki et al., 2011), and have been argued to reflect the syntactic and thematic complexity of unaccusatives. Syntactically, unaccusatives (on some models of grammar, such as Government and Binding; Chomsky, 1981) involve a movement operation, in which the Theme argument moves from an underlying object position to the subject position (The mani fell __i) (Burzio, 1986; Levin & Rappaport Hovav, 1995). Unaccusatives are also complex (and noncanonical) in terms of the mapping from thematic roles to syntax, given that the subject is assigned the Theme role. Similarly, object-experiencer verbs (e.g., The woman shocked the man) also contain a noncanonical argument order (subject = Theme; object = Experiencer) and have been argued to involve syntactic movement (Belletti & Rizzi, 1988). These have been shown to be impaired in agrammatic speakers (Thompson & Lee, 2009).

A distinct line of research has examined the effect of “semantic weight” on verb production in aphasia. This research contrasts production of semantically “heavy” verbs (e.g., bake), which have a clear and specific meaning, to semantically “light” verbs (e.g., get), which have a vaguer meaning and can appear in a variety of contexts. This research has demonstrated that agrammatism is associated with differential impairment of light verbs (Gordon & Dell, 2003; Thorne & Faroqi-Shah, 2016). According to the Division of Labor Hypothesis (Gordon & Dell, 2003), this is due to the complex argument structures and subcategorization frames associated with light verbs (e.g., get can appear in a wide range of syntactic contexts, e.g., get married, get to the party, get upset, get a haircut). In certain contexts, light verbs also require online composition of argument structure. For example, in a sentence such as John gave Bill an order to leave, the argument structures of give and order must be combined to yield the sentence’s interpretation, a process that is costly in typical language processing (Piñango, Mack, & Jackendoff, 2006; Wittenberg, Paczynski, Wiese, Jackendoff, & Kuperberg, 2014; Wittenberg & Piñango, 2011). Thus, impaired production of light verbs in agrammatism may also relate to difficulty with complex argument structures.

(p. 805) Sentence-Processing Deficits in Agrammatism

As mentioned in the introduction to this chapter, agrammatism is also associated with impairments in comprehending and producing complex syntactic structures, including sentences with embedding and/or a noncanonical order of arguments (see Bornkessel-Schlesewsky & Schlesewsky, Chapter 27 in this volume). This has been found in agrammatism caused by stroke (Bastiaanse & van Zonneveld, 2005; Burchert, Meissner, & De Bleser, 2008; Cho-Reyes & Thompson, 2012; Dragoy & Bastiaanse, 2010; Llinas-Grau & Martinez-Ferreiro, 2014; Thompson, Meltzer-Asscher, et al., 2013) and in PPA-G (Cupit et al., 2016; DeLeon et al., 2012; Thompson, Meltzer-Asscher, et al., 2013; Wilson, Dronkers, et al., 2010; Wilson, Henry, et al., 2010). Several theoretical accounts have been proposed of these deficits, which vary with respect to whether deficits are attributed to damaged linguistic representations, deficits in specific aspects of linguistic processing, or a general reduction in processing capacity (see recent reviews in Bastiaanse & Jonkers, 2012; Caplan, 2012; Druks, 2017; and Patil, Hanne, Burchert, De Bleser, & Vasishth, 2016).

One major focus of research has been to explain impaired comprehension of noncanonical sentences with long-distance dependencies (e.g., It was the girli whoi the boy kissed ___i that day at school). On some linguistic theories, these structures involve movement of a syntactic constituent (e.g., the relative pronoun who) from its original post-verbal position, leaving behind a gap or trace (___i) (Chomsky, 1981). In psycholinguistic terms, the filler (e.g., who, co-indexed with the girl) must be associated with the gap site (___i), or with its subcategorizing verb (e.g., kissed), in order to be assigned the correct thematic role (e.g., Theme) (Frazier, Clifton, & Randall, 1983; Pickering & Barry, 1991). Association of the filler with the gap site (or verb) involves reactivating aspects of the representation of the filler that have decayed since its original presentation (e.g., semantic representation; see review in Wagers & Phillips, 2014).

Some accounts have attributed impaired comprehension of these structures in agrammatism to impaired representation of syntactic movement (Grodzinsky, 1986, 2000). If correct, this hypothesis would predict the absence of reactivation of the meaning of the filler at the gap site. Studies of online processing have primarily tested this hypothesis using two methods: cross-modal priming, where reactivation is indicated by priming effects for the filler at the gap site, and visual-world eye-tracking, where reactivation is indicated through an increase in eye movements to a picture of the filler at the gap site. Although some early cross-modal priming studies found impaired filler-gap processing in agrammatism (Swinney, Zurif, Prather, & Love, 1995, 1996; Zurif, Swinney, Prather, Solomon, & Bushell, 1993), the majority of more recent priming and eye-tracking studies found intact filler-gap reactivation effects, albeit at a delay in some studies (Blumstein et al., 1998; Burkhardt, Piñango, & Wong, 2003; Dickey, Choy, & Thompson, 2007; Dickey & Thompson, 2009; Love, Swinney, Walenski, & Zurif, (p. 806) 2008; Thompson & Choy, 2009). Further, eye-tracking experiments conducted in our lab indicated intact processing in other types of long-distance dependencies, such as pronouns and reflexives (Choy & Thompson, 2010; Hsu & Thompson, 2014; Thompson & Choy, 2009), with no evidence of disrupted syntactic representation (contra, e.g., Grodzinsky, Wexler, Chien, Marakovitz, & Solomon, 1993).

Processing accounts of sentence comprehension deficits in agrammatism assume intact syntactic representations, but impaired processing of linguistic information. The Derived Order Problem Hypothesis (DOPH; Bastiaanse & van Zonneveld, 2006) agrees with researchers such as Grodzinsky (1986, 2000) that syntactic movement is the source of agrammatic comprehension deficits, but suggests that these deficits are processing based rather than representational. In contrast, other accounts suggest that processing slowdowns lead to comprehension deficits; specifically, slowed lexical activation (Love et al., 2008) or syntactic processing (Burkhardt et al., 2003) leads to the overuse of default sentence-interpretation strategies (e.g., subject = Agent). A third type of processing account suggests that a general reduction of processing resources leads to slowdowns and “intermittent deficiencies” (i.e., inconsistent syntactic operations; Caplan, Waters, DeDe, Michaud, & Reddy, 2007; Hanne, Sekerina, Vasishth, Burchert, & De Bleser, 2011).

We have argued that sentence comprehension deficits relate to impaired thematic integration (Mack et al., 2013; Mack & Thompson, 2017; Meyer, Mack, & Thompson, 2012; Thompson & Choy, 2009). This work follows the Mapping Hypothesis (Linebarger, Schwartz, & Saffran, 1983; Schwartz, Linebarger, Saffran, & Pate, 1987) in proposing a deficit in mapping between thematic and syntactic structure. However, our work also attempts to identify the specific processes that break down online during thematic integration. The relevant processes include thematic prediction and thematic role assignment.

As sentences unfold in real time, unimpaired listeners predict upcoming words and structures, supporting sentence comprehension by reducing time and resources needed for lexical and/or structural processing (Federmeier, 2007; Kamide, 2008; Kutas, DeLong, & Smith, 2011; Van Petten & Luka, 2012). In the domain of thematic processing, unimpaired listeners predictively assign the Agent role to sentence-initial animate noun phrases, in the absence of disambiguating grammatical (e.g., case) information (Hanne, Burchert, De Bleser, & Vasishth, 2015; Kamide, Scheepers, & Altmann, 2003; Knoeferle, Crocker, Scheepers, & Pickering, 2005; Meyer et al., 2012). For example, upon hearing a sentence starting with The woman, unimpaired listeners predict that the woman will be assigned the Agent role—a correct prediction if the sentence turns out to be active (e.g., The woman lifted the man), but incorrect if it is passive (e.g., The woman was lifted by the man). Notably, recent eye-tracking work in our lab and others’ shows that Agent-first predictions are absent in agrammatic listeners (Hanne et al., 2015; Mack & Thompson, 2017; Mack, Wei, Gutierrez, & Thompson, 2016; Meyer et al., 2012). Furthermore, restoring thematic prediction seems to be important for recovery of sentence comprehension in agrammatism. In a recent study, we used eye-tracking to examine changes in online sentence processing resulting from a course of language treatment in 10 individuals with agrammatism (Mack & Thompson, 2017). The language (p. 807) treatment protocol (Treatment of Underlying Forms [TUF]; Thompson & Shapiro, 2005) trained the production and comprehension of passive sentences. Although thematic prediction was not explicitly trained, participants nevertheless made more predictive eye movements following treatment. Further, the participants who showed greater increases in thematic prediction also showed greater improvement in sentence-comprehension accuracy.

In addition, thematic role assignment at the verb appears to be impaired in noncanonical sentences. For example, consider an object-cleft such as It was the girli whoi the boy kissed __i that day at school. Correct interpretation of this sentence requires assigning the boy the Agent role and the girl the Theme role (through its co-indexation with the gap and the relative pronoun who). As mentioned earlier, the majority of studies conducted to date suggest that agrammatic listeners can successfully compute the syntactic dependency, reactivating the filler (who = the girl) at the gap site. However, interpretation of the sentence is often incorrect, suggesting a subsequent failure to assign thematic roles correctly. Eye-tracking evidence is consistent with this hypothesis. For example, Dickey et al. (2007) found that listeners with agrammatism evinced eye movements indicative of successful syntactic dependency formation in object-wh questions, in sentences that were comprehended correctly as well as those comprehended incorrectly (cf. Dickey & Thompson, 2009; Thompson & Choy, 2009). In other words, syntactic dependency formation was generally successful, but thematic role assignment sometimes failed. Choy and Thompson (2010) reported a similar pattern of results in the processing of long-distance dependencies involving pronouns and reflexives: intact reactivation of the antecedent online, combined with impaired comprehension accuracy. Subsequent eye-tracking studies used a sentence-picture matching paradigm to probe incremental thematic role assignment during sentence comprehension. In sentences that were comprehended incorrectly, eye movements indicated aberrant thematic role processing throughout the sentence (Hanne et al., 2015; Hanne et al., 2011; Mack & Thompson, 2017; Mack et al., 2016; Meyer et al., 2012). These findings suggest that impaired thematic prediction and thematic role assignment play a key role in agrammatic comprehension deficits, leading to the Thematic Integration Hypothesis.

Moving to sentence production, some accounts propose that damage to syntactic representations underlies impairments in producing complex structures (Friedmann & Grodzinsky, 1997). However, as in sentence comprehension, there is evidence from sentence production that syntactic representations are intact. For example, agrammatic speakers show intact structural priming of complex structures; that is, they often use grammatical structures to which they have been recently exposed. This has been found for complex structures such as datives (Cho-Reyes et al., 2016; Hartsuiker & Kolk, 1998), passives (Cho & Thompson, 2010; Hartsuiker & Kolk, 1998), and cliticization in Italian (Rossi, 2015). Intact structural priming effects for complex structures also have been found in mixed groups of aphasic patients including agrammatic speakers (Saffran & Martin, 1997; Verreyt et al., 2013). Further, structural priming boosts production of complex structures in agrammatism. In one study (Cho-Reyes et al., 2016), 13 agrammatic (p. 808) speakers showed impaired production of dative sentences in isolation; however, in the context of a structural priming task, 7 of 13 speakers showed dative production accuracy within the normal range. These findings indicate that the representations of complex structures are intact.

Processing accounts vary with respect to the source of complex sentence production deficits. The Derived Order Problem Hypothesis, described earlier in the context of sentence comprehension, has also been applied to agrammatic production (Bastiaanse & van Zonneveld, 2005). This account claims that deficits stem from difficulty producing sentences with moved constituents. Other accounts propose more general processing impairments, such as a reduced sentence-planning window that poses difficulty for the production of complex sentences (Kolk, 1995). In contrast, we hypothesize that agrammatic speakers have difficulty with thematic integration during sentence production, which affects levels of processing including lexical selection, grammatical function assignment, and morphosyntactic encoding (see the model of Bock & Levelt, 1994) as well as the time course of sentence-production planning.

Lexical selection involves accessing and selecting lexical items (lemmas, containing semantic and syntactic but not phonological information) that encode an event’s meaning, including the action (typically a verb) and the event participants (typically nouns). Accessing a verb lemma activates its argument structure, including its thematic roles (e.g., Agent, Theme). As described in the previous section, research in our lab and others’ indicates that access to verbs with complex argument structures is particularly difficult for agrammatic speakers (e.g., Thompson, 2003). Grammatical function assignment concerns the mapping of selected lemmas to grammatical functions (subject, object). This process is guided by the argument structure information contained within verb lemmas: for example, some psychological verbs map the Experiencer to the subject role (e.g., John enjoyed the show) and others to the object role (e.g., The show amused John). Agrammatic speakers have deficits in using thematic information during grammatical function assignment, as reflected by difficulty in producing canonical active sentences with complex argument structures, such as two- and three-argument sentences (see previous section; e.g., Cho-Reyes & Thompson, 2012), as well as sentences with noncanonical argument order (discussed further in the following).

Morphosyntactic encoding refers to the generation of a hierarchically organized syntactic structure with morphologically specified words. The interplay between lexical selection, grammatical function assignment, and morphosyntactic encoding is especially important for complex sentence production. For example, to produce a passive sentence such as The man was lifted by the woman, the speaker must access the verb lift and its argument structure, map the Theme to the grammatical subject role and the Agent to an adjunct role, and select the correct morphosyntactic form of the verb (i.e., auxiliary + past participle). Establishing the relationship between grammatical function assignment and morphosyntactic encoding seems to be difficult for agrammatic speakers. When they are primed with the morphosyntactic structure of passives, they often produce role-reversal errors (i.e., incorrect grammatical function assignment; e.g., The woman was lifted by the man; Cho & Thompson, 2010) and when provided with a cue to (p. 809) map the Theme as the grammatical subject, they often produce morphosyntactic errors (e.g., The man was lifting by the woman; Faroqi-Shah & Thompson, 2003).

Further, agrammatic speakers often show abnormal sentence-planning processes, relating to impaired thematic integration. Two sentence-production planning modes have been observed in healthy speakers: verb-based structural planning, in which the speaker initially accesses the verb and uses it to build a structural frame that guides grammatical function assignment, and word-by-word incremental planning, in which the speaker first retrieves the most accessible noun and links it to the grammatical subject function. Healthy speakers use both modes of planning, depending on task demands and linguistic factors (Hwang & Kaiser, 2014; Kempen & Huijbers, 1983; J. Lee & Thompson, 2011a, 2011b; Schriefers, Teruel, & Meinshausen, 1998). Our preliminary work suggests that, unlike typical speakers, agrammatic speakers consistently retrieve verb information before speech onset, indicating verb-based structural planning (J. Lee & Thompson, 2011a, 2011b; J. Lee, Yoshida, & Thompson, 2015). For example, in two eye-tracking studies, speakers with agrammatism showed effects of argument structure complexity (e.g., encoding unaccusative vs. unergative verbs) before speech onset, whereas unimpaired speakers did so after speech onset (J. Lee & Thompson, 2011a, 2011b). This suggests a reliance on early retrieval of verb-argument structure information in agrammatic speakers, which is used to guide sentence planning (cf. J. Lee et al., 2015).

The use of structural planning may help agrammatic speakers manage the demands of sentence production, by temporally separating the costly processes of structural planning and articulation. However, faulty structural planning—that is, deficits in verb retrieval and mapping from thematic roles to syntactic structures—contribute to sentence-production deficits. In a recent eye-tracking study with nine agrammatic speakers (Mack, Nerantzini, & Thompson, 2017), we found evidence of abnormal structural planning during passive sentence production. However, after a course of Treatment of Underlying Forms (Thompson & Shapiro, 2005), which successfully trained passive sentence production, the agrammatic speakers showed more normal-like online sentence planning, reflecting improved thematic integration.

Neural Substrates of Verb- and Sentence-Processing Impairments in Agrammatism

Damage to left hemisphere frontal regions, posterior perisylvian regions, and dorsal white matter tracts have been consistently associated with agrammatism. In this section, we review the relevant findings regarding the neural substrates of verb- and sentence-processing impairments in agrammatism, situating them in the context of contemporary models of the neurobiology of language. We first discuss models of verb (p. 810) and verb-argument structure processing and follow this with sections on the neural mechanisms of sentence comprehension and sentence production, respectively.

Relatively few models have specifically addressed the neural substrates of verb and verb-argument structure processing. Thompson and Meltzer-Asscher (2014) proposed a model in which retrieval and integration of verb and verb-argument information is supported by a network consisting of left inferior parietal, posterior temporal, and inferior frontal regions. Early studies on stroke-induced aphasia suggested that verb-specific production deficits were related to left inferior frontal lesions, whereas noun-specific impairments were related to left temporal lesions (e.g., Damasio & Tranel, 1993; see review in Cappa & Perani, 2003; see also Kemmerer, Chapter 30 in this volume). However, more recent studies have shown that the neural substrates of verb-specific production deficits are more variable across individuals, and include lesions in left frontal, posterior temporal, and inferior parietal cortical regions, as well as damage to the insula, frontal operculum, dorsal white matter tracts, and/or subcortical structures such as the basal ganglia (e.g., Aggujaro, Crepaldi, Pistarini, Taricco, & Luzzatti, 2006; Kemmerer, Rudrauf, Manzel, & Tranel, 2012; Lukic et al., 2014; Piras & Marangolo, 2007; see reviews in Crepaldi, Berlingeri, Paulesu, & Luzzatti, 2011; Matzig, Druks, Masterson, & Vigliocco, 2009). Using voxel-based lesion symptom mapping (VLSM; Bates et al., 2003), we (Lukic et al., 2014) investigated the lesion locations associated with impaired production of argument structure. Impaired verb naming, measured with the Verb Naming Test of the Northwestern Assessment of Verbs and Sentences (NAVS; Thompson, 2011), was associated with lesions in the left IFG, STG, and insula; these effects were numerically stronger for transitive than for intransitive verbs, suggesting that these regions support the retrieval of verbs with complex argument structures. Further, we examined the neural correlates of impairments on the Argument Structure Production Test (ASPT) of the NAVS. In this task, participants viewed action pictures with the verb and event participants labeled (e.g., mail, man, letter) and were asked to produce a grammatical sentence to describe the picture, which requires mapping the arguments of the verb to the correct grammatical functions. Impaired performance on the ASPT was associated with damage to the SMG and arcuate fasciculus (AF). In PPA, few studies have directly examined the neural correlates of verb retrieval deficits. In recent work, we found that impaired verb-argument structure production on the ASPT is correlated with atrophy in the left inferior parietal lobule in a large group of patients with PPA (Europa, Mack, Rogalski, Mesulam, & Thompson, in preparation). In line with the model proposed by Thompson and Meltzer-Asscher (2014), these findings strongly suggest that dorsal pathways (i.e., linking posterior temporal, inferior parietal, and inferior frontal regions via the AF) play an important role in impaired production of verbs and verb-argument structure.

Sentence comprehension impairments in agrammatism are predominantly observed in semantically reversible and syntactically complex (e.g., noncanonical) sentences. Several studies have attempted to localize the brain damage associated with comprehension impairments of this nature. In the literature on chronic agrammatism resulting from stroke, this has resulted in mixed findings. One large-scale study of 79 patients (p. 811) found that impaired comprehension of semantically reversible sentences was associated with lesions in left posterior perisylvian regions, specifically the AG, SMG, and posterior STG (Thothathiri, Kimberg, & Schwartz, 2012). Greater impairment of noncanonical versus canonical sentences was associated with lesions in the left AG. Another large (72-patient) study related lesion location to comprehension of sentences that varied with respect to reversibility and complexity (Dronkers, Wilkins, Van Valin, Redfern, & Jaeger, 2004). In that study, lesions in the anterior STG, AG, and left frontal regions anterior to Broca’s area (BA 47 and BA 46) were associated with impaired sentence comprehension. Further, Caplan and colleagues observed relationships between syntactic complexity effects and lesions in the left posterior STG and AG, but not the IFG (Caplan, Michaud, Hufford, & Makris, 2016). These relationships were task- and structure-specific, suggesting that posterior perisylvian regions have distinct roles in carrying out syntactic operations in the contexts of particular tasks. In contrast, two previous studies by Caplan and colleagues found no significant relationships between lesion location and syntactic complexity effects on sentence comprehension (e.g., relatively impaired comprehension of passives vs. actives; Caplan et al., 1996; Caplan, Waters, Kennedy et al., 2007).

Further, a few studies have suggested that stroke-induced damage to the left IFG contributes to impaired predictive processing, which is important for sentence comprehension (Federmeier, 2007; Kamide, 2008; Kutas et al., 2011; Van Petten & Luka, 2012). In one study, clinically non-aphasic stroke survivors with left IFG lesions showed impaired prediction of morphosyntactic information (Jakuszeit, Kotz, & Hasting, 2013). In another study, aphasic individuals with left IFG lesions (but intact posterior perisylvian regions) showed impaired prediction of lexical-semantic and morpho-phonological information, whereas those with left posterior perisylvian lesions (but intact frontal regions) showed intact prediction (Nozari, Mirman, & Thompson-Schill, 2016). Similarly, we found that nine individuals with agrammatism and lesions that included left frontal regions showed impaired lexical-semantic prediction (Mack et al., 2013). These findings suggest that the left IFG supports linguistic prediction across domains. In future work, it will be important to test whether damage to this region is associated with impaired thematic prediction, which may contribute to deficits in sentence comprehension in agrammatism (Mack et al., 2013; Mack & Thompson, 2017; Mack et al., 2016; Meyer et al., 2012).

Studies conducted with PPA patients largely support those derived from stroke-induced aphasia. One large-scale study of 72 PPA patients found that impaired comprehension of semantically reversible, noncanonical sentences was associated with cortical atrophy in the left IFG, dorsal premotor cortex (DPM), and inferior parietal lobule (AG and SMG) (Mesulam, Thompson, Weintraub, & Rogalski, 2015). Generally consistent with this, another study reported an association between syntactic complexity effects (i.e., canonical>noncanonical difference scores) and atrophy in left frontal regions (IFG, DPM, and precentral gyrus [PCG]) as well as posterior temporal regions (left STG, middle temporal gyrus [MTG] and superior temporal sulcus [STS]) (Wilson, Dronkers, et al., 2010). A third study found an association between overall sentence comprehension (p. 812) impairment and atrophy in left posterior perisylvian regions, as well as a more specific association between deficits in comprehending complex (relative-clause) sentences and left IFG atrophy (Amici et al., 2007). A study by Peelle and colleagues on nonfluent PPA found relationships between impaired comprehension of complex sentences and cortical atrophy in left frontal regions (IFG, operculum, insula, dorsolateral frontal cortex), as well as the anterior STG (Peelle et al., 2008).

In addition to cortical regions, most current models of sentence comprehension also identify neural streams or pathways, that is, white matter tracts that connect cortical regions, including dorsal pathways (e.g., linking posterior temporal regions to inferior frontal regions via the parietal lobe, e.g., via the AF and superior longitudinal fasciculus [SLF]) and ventral pathways (e.g., linking posterior temporal cortex to the anterior temporal region via the temporal longitudinal fasciculus [TLF] and the inferior frontal cortex via the uncinate fasciculus [UF] and inferior frontal-occipital fasciculus [IFOF]) (Catani, Jones, & Ffytche, 2005). Both the dorsal and ventral pathways have been argued to play a role in sentence comprehension, but the specific functions of the two routes vary across models. Dorsal pathways, connecting posterior temporal to inferior frontal regions, via the AF, have been argued to support processing of complex syntactic structures (Friederici, 2012; Friederici & Gierhan, 2013) or syntactic processing in general (Bornkessel-Schlesewsky & Schlesewsky, 2013; Hagoort & Indefrey, 2014). Because stroke-induced aphasia often is associated with marked disruption of white matter tracts, researchers have turned to PPA to examine the relation between tract integrity and language ability. In PPA, white matter tracts often are only partially compromised, allowing for such analyses. Indeed, associations between damage to dorsal routes (i.e., the AF and SLF) and impaired comprehension have been reported in PPA (Wilson et al., 2011). Catani and colleagues (2017) found that, while both dorsal and ventral routes were disrupted in a group of 30 patients with PPA, correlations between sentence comprehension as tested by the NAVS (Thompson, 2011) and the posterior segment of the AF were noted. Functional neuroimaging (see Heim & Specht, Chapter 4 in this volume) studies of sentence comprehension have also supported these findings. One study reported that listeners with PPA-G, in contrast with unimpaired adults, did not show greater activation in the left IFG when comprehending noncanonical versus canonical sentences (Wilson, Dronkers, et al., 2010; cf. Cooke et al., 2003). Another study found that syntactic comprehension impairments were associated with abnormal functional activation in left frontal regions (IFG, insula, ventral PCG) as well as posterior temporal (MTG, STG) and inferior and superior parietal regions (i.e., dysfunction of regions within the dorsal route) (Wilson et al., 2016).

In contrast, ventral language pathways connecting temporal to frontal regions have been argued on several models to support semantic processing (Bornkessel-Schlesewsky & Schlesewsky, 2013; Hagoort & Indefrey, 2014) and appear to play little role in sentence-level deficits in PPA (Mandelli et al., 2014; Wilson, DeMarco, et al., 2014; Wilson et al., 2011). In the Catani et al. (2017) PPA study, ventral route (i.e., the UF and the TLF, but not the IFOF) disruptions were significantly correlated with single-word comprehension deficits. Some models, however, also propose a role for ventral pathways such as the (p. 813) UF in basic syntactic comprehension and phrase-structure building (Friederici, 2012; Friederici & Gierhan, 2013), as well as comprehension in general (Griffiths, Marslen-Wilson, Stamatakis, & Tyler, 2013; Hickok & Poeppel, 2015; Saur et al., 2008).

In contrast with sentence comprehension, relatively few studies have examined the neural correlates of impaired complex sentence production. In chronic agrammatism caused by stroke, we recently found that impaired sentence production (measured using the Sentence Production Priming Test of the NAVS) is associated with damage to the insula and inferior parietal regions (AG, SMG) (Lukic et al., 2014). Damage to the insula was specifically related to impairments in producing noncanonical (vs. canonical) sentences. Notably, Lukic et al. also found an association between lesions of the AF and sentence production. Turning to PPA, Rogalski and colleagues (Rogalski et al., 2011) used an anagram task to probe construction of complex sentences (the Northwestern Anagram Test [NAT]; Thompson, Weintraub, & Mesulam, 2012) and found that impaired performance was associated with atrophy in cortical regions including the anterior and posterior IFG, the ventral PCG and post-central gyrus, and the SMG. A study involving structured spoken sentence production found that impaired performance was associated with atrophy in the posterior IFG (DeLeon et al., 2012). In a study of narrative language production, atrophy in the IFG and surrounding frontal regions (e.g., the supplementary motor area [SMA]) was associated with reduced production of complex sentences with embedding, as well as a lower “syntactic composite” score (i.e., a principal component incorporating the rate of syntactic errors and the proportion of words occurring outside of sentences) (Wilson, Henry, et al., 2010). Further, dorsal language tracts have also been argued to play a particularly important role in language production (Hickok & Poeppel, 2015; Saur et al., 2008). Two studies found that damage to the AF/SLF was associated with impaired syntactic production (Mandelli et al., 2014; Wilson et al., 2011). One of these studies also implicated a second dorsal language pathway, connecting the left posterior IFG to the left SMA, in impaired sentence production, consistent with the claim that this pathway supports word sequencing (Mandelli et al., 2014). The role of this pathway in word sequencing may be specific to spoken-language production. Catani et al. (2013) examined the language functions of the left frontal aslant tract, which partially overlaps with the IFG-SMA pathway investigated by Mandelli et al. (2014). Catani and colleagues found that damage to the frontal aslant tract was associated with impaired fluency, but not with grammatical impairments. However, the grammatical production task used by Catani and colleagues was an anagram task (the Northwestern Anagram Test; Thompson, Weintraub, & Mesulam, 2012), which does not require spoken-language production. In contrast, the study by Mandelli and colleagues did require spoken-language production, and did find an association between the IFG-SMA pathway and grammatical abilities.

In summary, the preponderance of evidence suggests that damage to cortical regions, all within the dorsal language pathways, underlies both verb and sentence deficits in agrammatism. These regions include the left posterior STG, inferior parietal regions (AG, SMG), and inferior frontal regions (IFG). Additionally, sentence production engages the insula, SMA, and ventral PCG. The extant literature also shows that (p. 814) segments of the AF connect these regions, with the posterior segment associated with verb and sentence comprehension and anterior regions associated with verb and sentence production, whereas ventral language pathways play a relatively minor role.

Conclusion

In this chapter, we have provided an overview of research pertaining to verb- and sentence-processing deficits in agrammatism and their neural correlates. In future work, we expect that the study of agrammatism will become increasingly dynamic, with an emphasis on understanding change over time in language function and its neural substrates. To this end, a growing body of research has examined the neural correlates of aphasia recovery in the acute and subacute stages (e.g., Saur et al., 2006) as well as treatment-related recovery of sentence comprehension and production in chronic agrammatism (Thompson, den Ouden, Bonakdarpour, Garibaldi, & Parrish, 2010; Thompson, Riley, den Ouden, Meltzer-Asscher, & Lukic, 2013; Wierenga et al., 2006). Future work on recovery in stroke-induced agrammatism will likely also incorporate insights from theories of language (re)-learning in this population (Christiansen, Louise Kelly, Shillcock, & Greenfield, 2010; Goschke, Friederici, Kotz, & van Kampen, 2001; Schuchard, Nerantzini, & Thompson, 2017; Schuchard & Thompson, 2014, 2017; Zimmerer, Cowell, & Varley, 2014). A dynamic perspective is also necessary for understanding the mechanisms of language decline in agrammatic PPA, and how agrammatism can be effectively treated in the context of neurodegenerative disease (e.g., Hameister, Nickels, Abel, & Croot, 2017; Schneider, Thompson, & Luring, 1996).

In addition, developing a dynamic understanding of agrammatism will require integrating insights from studies using a wide range of methods (e.g., offline behavioral methods, eye-tracking, ERP, and neuroimaging measures of brain structure and function). In addition to the neuroimaging methods discussed here (i.e., structural measures of gray- and white-matter integrity, functional MRI), a fully specified model of agrammatism will also need to incorporate information about perfusion (cerebral blood flow; Thompson et al., 2010; Thompson et al., 2017) and functional and effective connectivity (e.g., den Ouden et al., 2012; Xiang, Fonteijn, Norris, & Hagoort, 2010). Thus, while much has already been accomplished in understanding the neurocognitive mechanisms of agrammatism, there is still much work to be done.

Acknowledgments

This research was funded by NIH R01-DC001948 (Thompson), P50-DC012283 (Thompson) and R01-DC008552 (Mesulam). We would like to thank our research participants, their families and caregivers, and our colleagues in the Aphasia and Neurolinguistics Research (p. 815) Laboratory, Center for the Neurobiology of Language Recovery, and the Cognitive Neurology and Alzheimer’s Disease Center at Northwestern University for their contributions to this work.

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