Unique semantic space in the brain of each beholder predicts perceived similarity

Abstract

The unique way in which each of us perceives the world must arise from our brain representations. If brain imaging could reveal an individual's unique mental representation, it could help us understand the biological substrate of our individual experiential worlds in mental health and disease. However, imaging studies of object vision have focused on commonalities between individuals rather than individual differences and on category averages rather than representations of particular objects. Here we investigate the individually unique component of brain representations of particular objects with functional MRI (fMRI). Subjects were presented with unfamiliar and personally meaningful object images while we measured their brain activity on two separate days. We characterized the representational geometry by the dissimilarity matrix of activity patterns elicited by particular object images. The representational geometry remained stable across scanning days and was unique in each individual in early visual cortex and human inferior temporal cortex (hIT). The hIT representation predicted perceived similarity as reflected in dissimilarity judgments. Importantly, hIT predicted the individually unique component of the judgments when the objects were personally meaningful. Our results suggest that hIT brain representational idiosyncrasies accessible to fMRI are expressed in an individual's perceptual judgments. The unique way each of us perceives the world thus might reflect the individually unique representation in high-level visual areas.visual perception | object representations | representational similarity analysis | neuroimaging | memory E veryone's perception of the world is unique. Psychologists and psychotherapists, using methods including questionnaires and free association, have long attempted to peer into an individual's subjective experiential world. The unique aspects of our experience coexist with a shared experiential component. We can all recognize the objects that surround us and name them in a common language. Consistent with this shared component of experience, there is evidence that visual stimuli are processed similarly in the brains of different individuals (1). However, the unique way in which each of us perceives an object also must arise from brain activity. Is there an individually unique component to our brain representations?Unidimensional aspects of subjective visual percepts, ranging from estimates of object size, color, vividness, and emotional valence, have separately been found to correlate with interindividual variation in both univariate regional-average activation and cortical anatomy (2, 3). However, it remains unclear how a person's multidimensional subjective percept reflects the multivariate brainactivity pattern that represents a particular object.Functional magnetic resonance imaging (fMRI) studies of object vision have focused largely on commonalities among subjects and category averages across particular stimuli. These studies have revealed regions in human inferior temporal ...

Semantic representations in the temporal pole predict false memories

“…Given that we rely on shared semantic representation to communicate with one another, this individual variation is perhaps surprising. However, it does converge with other recent reports of individual differences in semantic (30) and episodic representation (38), and suggests that divergent personal experience is sufficient to create individually unique representations in higher-level semantic regions. This striking finding suggests that it will be important to further characterize both the shared and individually unique aspects of semantic cognition to better understand the nature of conceptual knowledge.…”

“…4). Such a result cannot be explained by incidental differences in TP physiology or anatomy alone (30), as these more basic properties would not predict each subject's false-memory behavior.…”

“…We also investigated the possibility that subject-specific TP neural coding might predict true memory performance, using an individuation analysis (30). This analysis demonstrated a significant individuation effect in the TP for true memories (Z = 2.16, P = 0.016) as well as false memories, and this result remained significant after partialling out the three control variables (Z = 2.11, P = 0.017).…”

“…To assess this issue we used an individuation analysis (30), comparing the within-subject neural-behavioral correlations (unique semantic information) to the between-subject neural-behavioral correlations (shared semantic information), in each case controlling for the canonical false-memory strength to remove additional shared semantic information. This analysis revealed a significantly higher within-than between-subject correlation (Z = 2.63, P = 0.0042).…”

“…To test for the presence of unique TP neural information that predicts subject-specific false memories, we used an individuation analysis (30). The logic here is that if an individual has a unique set of TP neural representations that meaningfully influences cognition, then that individual's neural overlap data should predict their own pattern of falsememory errors better than any other subject's false-memory errors.…”