4.8 Article

Cortical ensembles selective for context

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2026179118

Keywords

predictive coding; circuits; neocortex

Funding

  1. National Institute of Mental Health [F32-MH106265, R00MH115082, R01MH115900]
  2. National Eye Institute Grant [R01EY011787]
  3. National Institute of General Medical Sciences Grant [T32GM008798-17]
  4. Howard Hughes Medical Institute student research fellowship
  5. Brains and Behavior Research Foundation [19944]
  6. Whitehall Foundation [2019-05-44]
  7. Burroughs Wellcome Fund [CASI 1015761]

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Neural processing of sensory information is strongly influenced by context, with stimulus-evoked responses being reduced or increased depending on contextual regularities. Deviance-augmented responses are limited to specific neurons in the supragranular layers of the visual cortex, forming a neuronal ensemble. Higher cortical areas modulate these context-selective ensembles in the primary sensory cortex, which play a crucial role in the brain's construction and selection of prediction errors.
Neural processing of sensory information is strongly influenced by context. For instance, cortical responses are reduced to predictable stimuli, while responses are increased to novel stimuli that deviate from contextual regularities. Such bidirectional modulation based on preceding sensory context is likely a critical component or manifestation of attention, learning, and behavior, yet how it arises in cortical circuits remains unclear. Using volumetric two-photon calcium imaging and local field potentials in primary visual cortex (V1) from awake mice presented with visual oddball paradigms, we identify both reductions and augmentations of stimulus-evoked responses depending, on whether the stimulus was redundant or deviant, respectively. Interestingly, deviance-augmented responses were limited to a specific subset of neurons mostly in supragranular layers. These deviance-detecting cells were spatially intermixed with other visually responsive neurons and were functionally correlated, forming a neuronal ensemble. Optogenetic suppression of prefrontal inputs to V1 reduced the contextual selectivity of deviance-detecting ensembles, demonstrating a causal role for top-down inputs. The presence of specialized context-selective ensembles in primary sensory cortex, modulated by higher cortical areas, provides a circuit substrate for the brain's construction and selection of prediction errors, computations which are key for survival and deficient in many psychiatric disorders.

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