Orthogonality of sensory and contextual categorical dynamics embedded in a continuum of responses from the second somatosensory cortex

Abstract

AbstractHow does the brain simultaneously process signals that bring complementary information, like raw sensory signals and their transformed counterparts, without any disruptive interference? Contemporary research underscores the brain’s adeptness in using decorrelated responses to reduce such interference. Both neurophysiological findings and artificial neural networks (ANNs) support the notion of orthogonal representation for signal differentiation and parallel processing. Yet, where, and how raw sensory signals are transformed into more abstract representations remains unclear. Using a temporal discrimination pattern task (TDPT) in trained monkeys, we revealed that the second somatosensory cortex (S2) efficiently segregates faithful and transformed neural responses into orthogonal subspaces. Importantly, S2 population encoding for transformed signals, but not for faithful ones, disappeared during a non-demanding version of the task, which suggests that signal transformation and their decoding from downstream areas are only active on-demand. A mechanistic computation model points to gain modulation as a possible biological mechanism for the observed context-dependent computation. Furthermore, individual neural activities that underlie the orthogonal population representations exhibited a continuum of responses, with no well-determined clusters. These findings advocate that the brain, while employing a continuum of heterogeneous neural responses, splits population signals into orthogonal subspaces in a context-dependent fashion to enhance robustness, performance, and improve coding efficiency.SIGNIFICANCE STATEMENTAn important function of the brain is turning sensation into perception. Yet, how this function is implemented remains unknown. Current research, coupled with insights from artificial neural networks, highlights using of orthogonal representations as an effective means to transform sensory signals into perceptual signals while separating and simultaneously processing the two information streams. Neuronal recordings in second somatosensory cortex (S2), obtained from monkeys performing a demanding vibrotactile discrimination task, revealed that this function is implemented at the population level. While S2 consistently encodes sensory inputs, the representation of transformed signals is contingent on task demand. Such distinct and flexible organization, enriched by a broad spectrum of neural activities, reflects the brain’s efficiency, resilience, and overall purpose for solving cognitive tasks.