The emergence of semantic meaning in the ventral temporal pathway

Abstract

In the ventral visual pathway, early visual areas encode light patterns on the retina in terms of image properties, for example, edges and color, whereas higher areas encode visual information in terms of objects and categories. At what point does semantic knowledge, as instantiated in human language, emerge? We examined this question by studying whether semantic similarity in language relates to the brain's organization of object representations in inferior temporal cortex (ITC), an area of the brain at the crux of several proposals describing how the brain might represent conceptual knowledge. Semantic relationships among words can be viewed as a geometrical structure with some pairs of words close in their meaning (e.g., man and boy) and other pairs more distant (e.g., man and tomato). ITC's representation of objects similarly can be viewed as a complex structure with some pairs of stimuli evoking similar patterns of activation (e.g., man and boy) and other pairs evoking very different patterns (e.g., man and tomato). In this study, we examined whether the geometry of visual object representations in ITC bears a correspondence to the geometry of semantic relationships between word labels used to describe the objects. We compared ITC's representation to semantic structure, evaluated by explicit ratings of semantic similarity and by five computational measures of semantic similarity. We show that the representational geometry of ITC—but not of earlier visual areas (V1)—is reflected both in explicit behavioral ratings of semantic similarity and also in measures of semantic similarity derived from word usage patterns in natural language. Our findings show that patterns of brain activity in ITC not only reflect the organization of visual information into objects but also represent objects in a format compatible with conceptual thought and language.