Thematic knowledge, artifact concepts, and the left posterior temporal lobe: Where action and object semantics converge

Abstract

Converging evidence supports the existence of functionally and neuroanatomically distinct taxonomic (similarity-based; e.g., hammer-screwdriver) and thematic (event-based; e.g., hammer-nail) semantic systems. Processing of thematic relations between objects has been shown to selectively recruit the left posterior temporoparietal cortex. Similar posterior regions have been also been shown to be critical for knowledge of relationships between actions and manipulable human-made objects (artifacts). Based on the hypothesis that thematic relationships for artifacts are based, at least in part, on action relationships, we assessed the prediction that the same regions of the left posterior temporoparietal cortex would be critical for conceptual processing of artifact-related actions and thematic relations for artifacts. To test this hypothesis, we evaluated processing of taxonomic and thematic relations for artifact and natural objects as well as artifact action knowledge (gesture recognition) abilities in a large sample of 48 stroke patients with a range of lesion foci in the left hemisphere. Like control participants, patients identified thematic relations faster than taxonomic relations for artifacts, whereas they identified taxonomic relations faster than thematic relations for natural objects. Moreover, response times for identifying thematic relations for artifacts selectively predicted performance in gesture recognition. Whole brain Voxel Based Lesion-Symptom Mapping (VLSM) analyses and Region of Interest (ROI) regression analyses further demonstrated that lesions to the left posterior temporal cortex, overlapping with LTO and visual motion area hMT+, were associated both with relatively slower response times in identifying thematic relations for artifacts and poorer artifact action knowledge in patients. These findings provide novel insights into the functional role of left posterior temporal cortex in thematic knowledge, and suggest that the close association between thematic relations for artifacts and action representations may reflect their common dependence on visual motion and manipulation information.

Sensory and semantic activations evoked by action attributes of manipulable objects: Evidence from ERPs

“…These differences may help explain the N400 scalp distributions that differed somewhat across the studies (ranging from frontal-central in, e.g., van Elk et al, 2010 to more clearly frontal, as in the current study). More generally, however, the relatively anterior N400 action-related priming effects seen in the present study and related previous studies suggest that access to action semantics (Bach et al, 2009; van Elk et al, 2008, 2010; also see Leshinskaya and Caramazza, 2016 for a discussion) may differ from access to semantic information with weaker relationships to sensory-motor attributes, such as seen in the taxonomic conditions here (see also Kalénine and Buxbaum, 2016; Tsagkaridis et al, 2014). 3 …”

Taxonomic and thematic semantic systems.

“…Converging evidence from about a dozen independent studies makes a strong case for a specific neural dissociation between taxonomic and thematic semantics: anterior temporal lobes (ATL) are particularly important for taxonomic semantic processing and the temporo-parietal cortex (TPC) is particularly important for thematic semantic processing (Bedny et al, 2014; Davey et al, 2016; de Zubicaray et al, 2013; Geng & Schnur, 2016; Henseler et al, 2014; Kalénine & Buxbaum, 2016; Kalénine et al, 2009; Lee et al, 2014; Merck et al, 2014; Mirman & Graziano, 2012a; Schwartz et al, 2011; Tsagkaridis et al, 2014; Wamain et al, 2015). These studies include functional neuroimaging of neurologically typical adults, brain stimulation studies, and studies of individuals with neurogenic deficits of language and semantic memory.…”

“…In contrast, thematic relations may rely more strongly on location, motion, and functional action features, which are critical for determining how objects interact or relate to one another in scenes or events. For example, several studies linked thematic semantic with knowledge of object-use actions (Davey et al, 2016; Kalénine & Buxbaum, 2016; Tsagkaridis et al, 2014). On this view, taxonomic and thematic semantic systems are fundamentally of the same type, but differ in terms of which kinds of features contribute most strongly.…”

“…Lesion-symptom mapping studies of individuals with left hemisphere strokes have revealed an association between TPC lesions and deficits in recognition and production of meaningful gestures and object-use actions (Buxbaum, Shapiro, & Coslett, 2014; Kalénine, Buxbaum, & Coslett, 2010; Tarhan, Watson, & Buxbaum, 2015; for fMRI evidence see also Watson, Cardillo, Ianni, & Chatterjee, 2013). Particularly relevant to this proposal are explicit associations between deficits in thematic semantics and deficits in action knowledge (Kalénine & Buxbaum, 2016; see also Tsagkaridis et al, 2014). TPC regions are more strongly activated during semantic similarity judgments of action and event concepts compared to object concepts (Bedny et al, 2014; Kable, Kan, Wilson, Thompson-Schill, & Chatterjee, 2005; Kable, Lease-Spellmeyer, & Chatterjee, 2002).…”

Differential Tuning of Ventral and Dorsal Streams during the Generation of Common and Uncommon Tool Uses

“…First, a bilateral dorso-dorsal stream processes information related to aspects of tool orientation (e.g., the lateral occipital parietal junction; Valyear, Culham, Sharif, Westwood, & Goodale, 2006) and the kinematics of the arm and hand during online grasping (e.g., the anterior intraparietal sulcus; Culham et al, 2003; Chao & Martin, 2000; see Culham & Valyear, 2006, for a review). Second, a left-lateralized ventro-dorsal stream processes information both about characteristic visual tool motion (e.g., the posterior middle temporal gyrus; Kalénine & Buxbaum, 2016; Beauchamp, Lee, Haxby, & Martin, 2002, 2003; see Beauchamp & Martin, 2007, for a review) and about learned sensorimotor associations between tools and actions (e.g., supramarginal gyrus; see also Buxbaum & Kalénine, 2010, for a review). The role of these regions is confirmed by neuropsychological studies showing that damage to critical nodes of the ventro-dorsal stream in the left hemisphere produces behavioral impairments in tool use (Salazar-López, Schwaiger, & Hermsdörfer, 2016) and the execution and recognition of pantomimed tool use (apraxia; Goldenberg, Hartmann, & Schlott, 2003; see Buxbaum, Shapiro, & Coslett, 2014, for a review; see also Borra et al, 2008; Zhong & Rockland, 2003, for anatomical evidence in nonhuman primates).…”