Object recognition is enabled by an experience-dependent appraisal of visual features in the brain’s value system

• Published in: NeuroImage (Orlando, Fla.) Vol. 221; p. 117143
• Main Authors: Kozunov, Vladimir V., West, Timothy O., Nikolaeva, Anastasia Y., Stroganova, Tatiana A., Friston, Karl J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.11.2020; Elsevier Limited; Academic Press; Elsevier
• Subjects: Adult; Cerebral Cortex - physiology; Cortex (entorhinal); Female; Functional Neuroimaging - methods; Hemispheric laterality; Humans; Influence; Information processing; Judgment - physiology; Latency; Magnetoencephalography; Magnetoencephalography - methods; Male; Mooney figure disambiguation; Object recognition; Pattern recognition; Pattern Recognition, Visual - physiology; Perception; Predictive coding; Principles; Prior experience; Region-based multivariate pattern analysis; Representational similarity analysis; Semantics; Temporal cross-decoding generalization; Time Factors; Value system; Visual cortex; Visual perception; Visual stimuli; Young Adult; Temporal cross-decoding generalization; Magnetoencephalography; Mooney figure disambiguation; Predictive coding; Representational similarity analysis; Prior experience; Region-based multivariate pattern analysis; Object recognition; Value system; Visual perception
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2020.117143

This paper addresses perceptual synthesis by comparing responses evoked by visual stimuli before and after they are recognized, depending on prior exposure. Using magnetoencephalography, we analyzed distributed patterns of neuronal activity – evoked by Mooney figures – before and after they were recognized as meaningful objects. Recognition induced changes were first seen at 100–120 ​ms, for both faces and tools. These early effects – in right inferior and middle occipital regions – were characterized by an increase in power in the absence of any changes in spatial patterns of activity. Within a later 210–230 ​ms window, a quite different type of recognition effect appeared. Regions of the brain’s value system (insula, entorhinal cortex and cingulate of the right hemisphere for faces and right orbitofrontal cortex for tools) evinced a reorganization of their neuronal activity without an overall power increase in the region. Finally, we found that during the perception of disambiguated face stimuli, a face-specific response in the right fusiform gyrus emerged at 240–290 ​ms, with a much greater latency than the well-known N170m component, and, crucially, followed the recognition effect in the value system regions. These results can clarify one of the most intriguing issues of perceptual synthesis, namely, how a limited set of high-level predictions, which is required to reduce the uncertainty when resolving the ill-posed inverse problem of perception, can be available before category-specific processing in visual cortex. We suggest that a subset of local spatial features serves as partial cues for a fast re-activation of object-specific appraisal by the value system. The ensuing top-down feedback from value system to visual cortex, in particular, the fusiform gyrus enables high levels of processing to form category-specific predictions. This descending influence of the value system was more prominent for faces than for tools, the fact that reflects different dependence of these categories on value-related information. •Recognition effects following Mooney figure disambiguation were decoded from MEG data.•Neural changes occur in 3 stages that challenge the hierarchical view of perception.•Category-specific activity in the brain’s value system precedes that in visual cortex.•Face-specific response in the right fusiform gyrus is delayed for disambiguated faces.•The top-down influence of the value system is more prominent for faces than for tools.