Elsevier

Neuropsychologia

Volume 50, Issue 8, July 2012, Pages 1990-1997
Neuropsychologia

Damage to temporo-parietal cortex decreases incidental activation of thematic relations during spoken word comprehension

https://doi.org/10.1016/j.neuropsychologia.2012.04.024Get rights and content

Abstract

Both taxonomic and thematic semantic relations have been studied extensively in behavioral studies and there is an emerging consensus that the anterior temporal lobe plays a particularly important role in the representation and processing of taxonomic relations, but the neural basis of thematic semantics is less clear. We used eye tracking to examine incidental activation of taxonomic and thematic relations during spoken word comprehension in participants with aphasia. Three groups of participants were tested: neurologically intact control participants (N=14), individuals with aphasia resulting from lesions in left hemisphere BA 39 and surrounding temporo-parietal cortex regions (N=7), and individuals with the same degree of aphasia severity and semantic impairment and anterior left hemisphere lesions (primarily inferior frontal gyrus and anterior temporal lobe) that spared BA 39 (N=6). The posterior lesion group showed reduced and delayed activation of thematic relations, but not taxonomic relations. In contrast, the anterior lesion group exhibited longer-lasting activation of taxonomic relations and did not differ from control participants in terms of activation of thematic relations. These results suggest that taxonomic and thematic semantic knowledge are functionally and neuroanatomically distinct, with the temporo-parietal cortex playing a particularly important role in thematic semantics.

Highlights

► Examined activation of taxonomic and thematic semantic relations using eye-tracking. ► Compared participants with fronto-temporal or temporo-parietal lesions to controls. ► Posterior lesion group had reduced activation of thematic, not taxonomic, relations. ► Anterior lesion group had extended activation of taxonomic, not thematic, relations. ► Left temporo-parietal cortex is specialized for thematic semantic knowledge.

Introduction

Semantic knowledge consists of two broad kinds of relations: similarity and complementarity. Similarity is typically defined in terms of feature overlap, which can naturally give rise to categorical, or “taxonomic” structure (e.g., Rogers and McClelland, 2004, Rogers et al., 2004, O'Connor et al., 2009). Taxonomic semantic knowledge has been studied extensively in behavioral, neuropsychological, and functional imaging studies with an emerging consensus that anterior temporal lobe (ATL) structures play a particularly important role in the representation and processing of these relations (for a review, see Patterson, Nestor, & Rogers, 2007).

Complementary objects typically do not share features; rather they have complementary features that correspond to their complementary roles in events or situations. Complementarity can be defined as frequent occurrence in events or situations and we refer to these as “thematic” relations. Although thematic relations have been studied extensively in behavioral studies (for a review, see Estes, Golonka, & Jones, 2011), relatively little is known about their neural basis. Recent behavioral evidence suggests that taxonomic and thematic semantic knowledge may be somewhat distinct: Mirman and Graziano (in press) found that across 30 neurologically intact individuals, the incidental activation of taxonomically related concepts compared to thematically related concepts in a word recognition task predicted the tendency to choose the taxonomic option in an explicit, nonverbal semantic similarity judgment task. That is, individuals varied in their reliance on taxonomic vs. thematic knowledge across tasks (see also Simmons & Estes, 2008). This finding suggests that taxonomic and thematic knowledge comprise two parallel complementary semantic systems (for related work distinguishing concrete and abstract concepts see Crutch and Warrington, 2005, Crutch and Warrington, 2010). However, these results did not speak to the neural basis of these systems.

In a recent voxel-based lesion-symptom mapping (VLSM) study of picture naming errors produced by individuals with aphasia, Schwartz et al. (2011) found that participants generally produced far more taxonomic errors (coordinate, superordinate, or subordinate noun substitutions) than thematic errors (non-taxonomic errors that named an object that co-occurred with the target in the context of an action, event, or sentence), but the relative tendency to produce one error type vs. the other varied as a function of their lesion location. Individuals with lesions affecting the left anterior temporal lobe (ATL) produced a higher proportion of taxonomic errors relative to thematic errors and individuals with lesions affecting the left temporo-parietal cortex (TPC) produced a higher proportion of thematic errors relative to taxonomic errors.

The finding that ATL damage is associated with taxonomic errors is consistent with this region's well-documented importance for taxonomic semantics (e.g., Patterson et al., 2007, Schwartz et al., 2009, Walker et al., 2011; individuals with ATL degeneration produce almost exclusively taxonomic errors, but deficits in thematic semantic knowledge become evident when thematic relations are explicitly tested, e.g., Bozeat et al., 2000, Butler et al., 2009). In contrast, the finding that TPC damage is associated with thematic errors is quite novel, though at least one functional imaging study has identified this region as important for processing thematic relations (Kalénine et al., 2009; for a recent review of the neural basis of semantic memory see Binder & Desai, 2011). Schwartz et al. (2011) proposed a complementary semantic systems account, but there are at least two alternative interpretations of this result. The first is that TPC involvement in production of thematic picture naming errors is specific to picture naming or, slightly more generally, word production tasks and does not reflect core thematic semantic processing.

The second alternative is that thematic errors in picture naming are symptomatic of a cognitive control deficit and TPC is involved in cognitive control, rather than thematic semantics (e.g., Jefferies & Lambon Ralph, 2006). There is strong evidence that at least some individuals with aphasia have relatively general cognitive control deficits (Corbett et al., 2011, Hoffman et al., 2011, Jefferies and Lambon Ralph, 2006, Mirman et al., 2011, Noonan et al., 2010, Novick et al., 2009, Robinson et al., 1998, Schnur et al., 2009, Warrington and Cipolotti, 1996). These deficits have been associated with damage to the inferior frontal gyrus (IFG; e.g., Schnur et al., 2009), but Jefferies, Lambon Ralph and their colleagues have proposed that TPC damage may also cause cognitive control deficits. This proposal emerged from several studies in which patients with lesions encompassing both inferior frontal (IFG) and temporo-parietal (TPC) regions exhibited semantic control deficits. Further, patients with lesions restricted to one region or the other tended to show similar behavioral patterns of semantic control deficits (Corbett et al., 2011, Hoffman et al., 2011, Jefferies and Lambon Ralph, 2006, Noonan et al., 2010). The strongest evidence for a unique role of TPC in cognitive control processes comes from a recent TMS study (Whitney, Kirk, O'Sullivan, Lambon Ralph, & Jefferies, 2012), which suggested that this region is particularly important for top-down control of semantic retrieval, namely retrieving feature-specific information such as shape or color. Schwartz et al. (2011) considered this cognitive control account and ruled it out because (1) their measure of thematic error production controlled for controlled semantic retrieval as measured by the Camel and Cactus Test (Bozeat et al., 2000) and (2) production of the canonical “off-task” error type – semantic descriptions (horse → “it goes neigh”) – was associated with ATL damage only, not TPC damage. Thus, their results do not appear attributable to a TPC-based cognitive control deficit, but the extent to which TPC is involved in thematic semantics versus cognitive control remains an open question. The present study was designed to test the claim that TPC is specifically involved in thematic semantics and to evaluate the two alternative accounts.

Section snippets

Experiment

We tested the hypothesis that TPC is specifically involved in thematic semantics and the two alternative accounts using eye tracking to examine incidental activation of taxonomic and thematic knowledge during spoken word comprehension. We used a passive version of the “visual world paradigm” (Tanenhaus, Spivey-Knowlton, Eberhard, & Sedivy, 1995; cf. Cooper, 1974) in which pictures of four objects are presented on a computer screen and participants hear a word that matches one of the pictures1

Results

Fig. 3 shows the competitor fixation time courses separately for each of the three participant groups for the Thematic and Taxonomic condition. The full GCA results for the critical Object-x-Group interaction terms are shown in Table 2. In the Thematic condition, the Posterior group exhibited less overall semantic competition compared to the Control group (Intercept term: Estimate=-0.036, SE=0.016, p<0.05) and the competition emerged later in the time window (Cubic term: Estimate=−0.084, SE

General discussion

We used eye tracking to examine incidental activation of taxonomic and thematic relations during spoken word comprehension in participants with aphasia. Compared to neurologically intact control participants, individuals with lesions in BA 39 and surrounding temporo-parietal cortex (TPC) regions showed reduced and delayed activation of thematic relations, but not taxonomic relations. In contrast, individuals with the same degree of aphasia severity and semantic impairment resulting from lesions

Acknowledgments

This work was supported by National Institutes of Health grant R01DC010805 to DM and the Moss Rehabilitation Research Institute. A preliminary report was presented as a poster at the 2011 Neurobiology of Language Conference. We thank Myrna Schwartz and the Language and Aphasia lab at MRRI for helpful discussions and insightful suggestions.

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