Neural basis of semantic processing across comprehension contexts

Current neurobiological models of semantic cognition have been predominately derived from studies of single-words or sentences which may provide an impoverished estimate of how semantic processing occurs in real-world contexts. Studies that make use of more ecologically valid stimuli such as natural language or narratives suggest that, counter to the hub-and-spoke framework in which the anterior temporal lobe (ATL) serves as a graded hub integrating information from proximal sensorimotor spokes, the semantic system displays voxel-wise category specialization tiled across a large, distributed network. A complicating factor in reconciling these seemingly conflicting claims is the over-reliance on concrete conceptual knowledge in describing the organization of the semantic system. A recent theoretical account argues that social knowledge, like other types of semantic knowledge, is processed within the ventrolateral ATL, but this claim has not been tested using naturalistic stimuli, which better sample abstract social knowledge, including pragmatic inference. This thesis investigates the organization of the semantic system across multiple scales, from isolated words to multimodal narratives, and across multiple types of semantic conceptual knowledge, from concrete to abstract. Using comprehension of concrete words as a starting point, the first study describes a critical examination of specialization within the semantic system for taxonomic (dog – bear) and thematic (dog – leash) relations using intracranial EEG recordings from an array of depth electrodes within ATL, inferior parietal lobule (IPL), and two regions within the semantic control network, inferior frontal gyrus (IFG) and posterior middle temporal gyrus (pMTG). Moving across the context and conceptual scale to build upon this work, the second study investigated how the concrete and abstract lexical and semantic properties of single-words, akin to those that informed the hub-and-spoke model, are processed in a complex, complete narrative presented to participants during fMRI scanning. In doing so, this study enabled comparisons between prior studies of isolated words and naturalistic work, thus moving toward an integrated cross-scale account of semantic cognition. Using the same neuroimaging data, the third study extended this work to investigate how context contributes to the construction of meaning by studying how the semantic and social cognitive systems are engaged by social and pragmatic sentence-level content. This enabled a direct, naturalistic test of the claim that social knowledge is housed within the semantic system. The fourth study investigated shared processing between social and semantic systems using fMRI data collected during movie-viewing, which captures the multimodal environment in which social knowledge is exchanged. The results of these studies collectively demonstrate that the semantic and social systems are differentially engaged across the scales investigated here. Concrete conceptual relations engage one (or more) specialized hubs within the semantic system, whereas processing of naturalistic verbal and event content co-varies with activation in large brain networks. There is evidence of functional gradations within ATL that are differentially sensitive to the demands of narrative comprehension – the anterior superior temporal gyrus (i.e., dorsolateral subregion) and anterior fusiform (i.e., ventral subregion) appear to be particularly sensitive to the quantity and informativeness of external input whereas the anterior middle and inferior temporal gyri (i.e., ventrolateral subregion) appear to be engaged by internal, or endogenous, semantic processing during narrative comprehension. Engagement of this same ventrolateral subregion is observed in response to social word and sentence content, providing support for the claim that social processing is subsumed within the semantic system. Taken together, the results suggest an extension to the current neurobiological model of semantic cognition that accommodates comprehension contexts. The studies undertaken as part of this thesis build upon the existing concept-level frameworks towards a narrative-level framework of semantic cognition.