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Transformation of primary sensory cortical representations from layer 4 to layer 2.

ABSTRACT: Sensory input arrives from thalamus in cortical layer (L) 4, which outputs predominantly to superficial layers. L4 to L2 thus constitutes one of the earliest cortical feedforward networks. Despite extensive study, the transformation performed by this network remains poorly understood. We use two-photon calcium imaging to record neural activity in L2-4 of primary vibrissal somatosensory cortex (vS1) as mice perform an object localization task with two whiskers. Touch responses sparsen and become more reliable from L4 to L2, with nearly half of the superficial touch response confined to ~1 % of excitatory neurons. These highly responsive neurons have broad receptive fields and can more accurately decode stimulus features. They participate disproportionately in ensembles, small subnetworks with elevated pairwise correlations. Thus, from L4 to L2, cortex transitions from distributed probabilistic coding to sparse and robust ensemble-based coding, resulting in more efficient and accurate representations.

SUBMITTER: Voelcker B

PROVIDER: S-EPMC9485231 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Transformation of primary sensory cortical representations from layer 4 to layer 2.

Voelcker Bettina B Pancholi Ravi R Peron Simon S

Nature communications 20220919 1

Sensory input arrives from thalamus in cortical layer (L) 4, which outputs predominantly to superficial layers. L4 to L2 thus constitutes one of the earliest cortical feedforward networks. Despite extensive study, the transformation performed by this network remains poorly understood. We use two-photon calcium imaging to record neural activity in L2-4 of primary vibrissal somatosensory cortex (vS1) as mice perform an object localization task with two whiskers. Touch responses sparsen and become ...[more]

PMID: 36123376

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Project description:Cortical areas have the capacity of large-scale reorganization following sensory deafferentation. However, it remains unclear whether this phenomenon is a unique process that homogeneously affects the entire deprived cortical region or whether it is susceptible to changes depending on neuronal networks across distinct cortical layers. Here, we studied how the local circuitry within each layer of the deafferented cortex forms the basis for neuroplastic changes after immediate thoracic spinal cord injury (SCI) in anaesthetized rats. In vivo electrophysiological recordings from deafferented hindlimb somatosensory cortex showed that SCI induces layer-specific changes mediating evoked and spontaneous activity. In supragranular layer 2/3, SCI increased gamma oscillations and the ability of these neurons to initiate up-states during spontaneous activity, suggesting an altered corticocortical network and/or intrinsic properties that may serve to maintain the excitability of the cortical column after deafferentation. On the other hand, SCI enhanced the infragranular layers' ability to integrate evoked sensory inputs leading to increased and faster neuronal responses. Delayed evoked response onsets were also observed in layer 5/6, suggesting alterations in thalamocortical connectivity. Altogether, our data indicate that SCI immediately modifies the local circuitry within the deafferented cortex allowing supragranular layers to better integrate spontaneous corticocortical information, thus modifying column excitability, and infragranular layers to better integrate evoked sensory inputs to preserve subcortical outputs. These layer-specific neuronal changes may guide the long-term alterations in neuronal excitability and plasticity associated with the rearrangements of somatosensory networks and the appearance of central sensory pathologies usually associated with spinal cord injury. KEY POINTS: Sensory stimulation of forelimb produces cortical evoked responses in the somatosensory hindlimb cortex in a layer-dependent manner. Spinal cord injury favours the input statistics of corticocortical connections between intact and deafferented cortices. After spinal cord injury supragranular layers exhibit better integration of spontaneous corticocortical information while infragranular layers exhibit better integration of evoked sensory stimulation. Cortical reorganization is a layer-specific phenomenon.

Dataset Information

Transformation of primary sensory cortical representations from layer 4 to layer 2.

Publications

Transformation of primary sensory cortical representations from layer 4 to layer 2.

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