The neurobiology of semantic memory

Abstract

Semantic memory includes all acquired knowledge about the world and is the basis for nearly all human activity, yet its neurobiological foundation is only now becoming clear. Recent neuroimaging studies demonstrate two striking results: the participation of modality-specific sensory, motor, and emotion systems in language comprehension, and the existence of large brain regions that participate in comprehension tasks but are not modality-specific. These latter regions, which include the inferior parietal lobe and much of the temporal lobe, lie at convergences of multiple perceptual processing streams. These convergences enable increasingly abstract, supramodal representations of perceptual experience that support a variety of conceptual functions including object recognition, social cognition, language, and the remarkable human capacity to remember the past and imagine the future.

Figure 1. Modality-specific activation peaks during language comprehension

This figure displays sites of peak activation from 38 imaging studies that examined modality-specific knowledge processing during language comprehension tasks. Peaks were mapped to a common spatial coordinate system and then to a representative brain surface. Action knowledge peaks (red) cluster in primary and secondary sensorimotor regions in the posterior frontal and anterior parietal lobes. Motion peaks (green) cluster in posterior inferolateral temporal regions near the visual motion processing pathway. Note that motion concepts, especially when elicited by action verbs, are difficult to distinguish from action concepts. Peaks near motion processing area MT/MST in four of the studies of action language are interpreted here as reflecting motion knowledge. Auditory peaks (yellow) occur in superior temporal and temporoparietal regions adjacent to auditory association cortex. Color peaks (blue) cluster in the fusiform gyrus just anterior to color-selective regions of extrastriate visual cortex. Olfactory peaks (pink) observed in one study were in olfactory areas (prepiriform cortex and amygdala). Gustatory peaks (orange) were observed in one study in the anterior orbital frontal cortex. Emotion peaks (purple) involve primarily anterior temporal, medial and orbital prefrontal, and posterior cingulate regions. Details regarding study selection and a list of the included studies are provided in supplementary material online.

Figure 2. Meta-analysis of functional imaging studies of semantic processing

This figure displays brain regions reliably activated by general semantic processes, based on reported activation peaks from 120 independent functional imaging studies (p <.05 corrected for family-wise error). The analysis method assigns a significance value to the degree of spatial overlap between the reported activation coordinates in a standard volume space. The figure shows selected sagittal sections in the left hemisphere; right hemisphere activations occurred in similar locations but were less extensive. AG = angular gyrus, FG = fusiform gyrus, IFG = inferior frontal gyrus, MTG = middle temporal gyrus, PC = posterior cingulate gyrus, SFG = superior frontal gyrus, SMG = supramarginal gyrus, VMPFC = ventromedial prefrontal cortex. Green lines indicate the Y and Z axes in standard space. Adapted from [47].

Figure 3. Possible relationships between perceptual and conceptual representation

Theories of perception and cognition vary in terms of the degree of separation between these processes. Disembodied models propose a complete separation, in which conceptual processing is based entirely on amodal, symbolic representations [9, 10, 17]. Other theories propose that conceptual and perceptual representations are distinct and separate but interact closely so that amodal symbols can derive content from perceptual knowledge [7, 14]. In contrast to both of these theories, strong embodiment models posit that perceptual and conceptual processes are carried out by a single system [55, 56]. In contrast to all of these theories, the neuroanatomical evidence for multiple modality-specific systems gradually converging on a common semantic network suggests a process of `embodied abstraction,' in which conceptual representation is embodied in multiple levels of abstraction from sensory, motor and affective input. The extent to which modality-specific perceptual representations are activated during semantic tasks varies with concept familiarity, demand for perceptual information and degree of contextual support (see Box 1).

Figure 4. A neuroanatomical model of semantic processing

A model of semantic processing in the human brain is shown, based on a broad range of pathological and functional neuroimaging data. Modality-specific sensory, action, and emotion systems (yellow regions) provide experiential input to high-level temporal and inferior parietal convergence zones (red regions) that store increasingly abstract representations of entity and event knowledge. Dorsomedial and inferior prefrontal cortices (blue regions) control the goal-directed activation and selection of the information stored in temporoparietal cortices. The posterior cingulate gyrus and adjacent precuneus (green region) may function as an interface between the semantic network and the hippocampal memory system, helping to encode meaningful events into episodic memory. A similar, somewhat less extensive semantic network exists in the right hemisphere, although the functional and anatomical differences between left and right brain semantic systems are still unclear.