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J Neurosci. 2019 Mar 13;39(11):2052-2064. doi: 10.1523/JNEUROSCI.1459-18.2018. Epub 2019 Jan 16.

Superficial Layers Suppress the Deep Layers to Fine-tune Cortical Coding.

Author information

1
Department of Molecular and Cell Biology and the Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720, and.
2
Department of Biology, Purdue University, West Lafayette, Indiana 47907.
3
Department of Biology, Purdue University, West Lafayette, Indiana 47907 hadesnik@berkeley.edu.

Abstract

The descending microcircuit from layer 2/3 (L2/3) to layer 5 (L5) is one of the strongest excitatory pathways in the cortex, presumably forming a core component of its feedforward hierarchy. To date, however, no experiments have selectively tested the impact of L2/3 activity on L5 during active sensation. We used optogenetic, cell-type-specific manipulation of L2/3 neurons in the barrel cortex of actively sensing mice (of either sex) to elucidate the significance of this pathway to sensory coding in L5. Contrary to standard models, activating L2/3 predominantly suppressed spontaneous activity in L5, whereas deactivating L2/3 mainly facilitated touch responses in L5. Somatostatin interneurons are likely important to this suppression because their optogenetic deactivation significantly altered the functional impact of L2/3 onto L5. The net effect of L2/3 was to enhance the stimulus selectivity and expand the range of L5 output. These data imply that the core cortical pathway increases the selectivity and expands the range of cortical output through feedforward inhibition.SIGNIFICANCE STATEMENT The primary sensory cortex contains six distinct layers that interact to form the basis of our perception. While rudimentary patterns of connectivity between the layers have been outlined quite extensively in vitro, functional relationships in vivo, particularly during active sensation, remain poorly understood. We used cell-type-specific optogenetics to test the functional relationship between layer 2/3 and layer 5. Surprisingly, we discovered that L2/3 primarily suppresses cortical output from L5. The recruitment of somatostatin-positive interneurons is likely fundamental to this relationship. The net effect of this translaminar suppression is to enhance the selectivity and expand the range of receptive fields, therefore potentially sharpening the perception of space.

KEYWORDS:

active sensing; circuits; cortex; receptive fields; sensory coding; translaminar

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