Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation

Abstract

Visual deprivation during a developmental sensitive period markedly alters visual cortical response properties, but the changes in intracortical circuitry that underlie these effects are poorly understood. Here we use a slice preparation of rat primary visual cortex to show that 2 d of prior visual deprivation early in life increases the excitability of layer 4 circuitry. Slice recordings showed that spontaneous activity of layer 4 star pyramidal neurons increased 25-fold after 2 d of visual deprivation between postnatal days (P) 15 and P17. This effect was mediated by increased net excitatory and decreased net inhibitory synaptic drive. Paired recordings showed that excitatory connections between star pyramidal neurons doubled in amplitude, whereas inhibitory connections decreased or increased depending on the interneuron class. These effects reversed when vision was restored. This dynamic adjustment of the excitation-inhibition balance may allow the networks within layer 4 to maintain stable levels of activity in the face of variable sensory input.

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Figure 1: Spontaneous activity of layer 4 star pyramidal neurons was increased after 2 d of visual deprivation.
Figure 2: Visual deprivation did not affect the intrinsic excitability of star pyramidal neurons.
Figure 3: The balance between excitatory and inhibitory synaptic drive was altered by visual deprivation.
Figure 4: Visual deprivation increased the amplitude of monosynaptic connections between star pyramidal neurons.
Figure 5: Visual deprivation decreased the amplitude of monosynaptic connections between fast-spiking and star pyramidal neurons.
Figure 6: Visual deprivation increased the amplitude of monosynaptic connections between RSNP and star pyramidal neurons but decreased the connection probability.

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Acknowledgements

We thank R. Cudmore for help with software, J. Barry and K. Essig for histology and S. Fusi and X.-J. Wang for helpful discussions. Supported by the National Eye Institute (EY014439) and the National Institute on Drug Abuse (DA16455).

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Correspondence to Gina G Turrigiano.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Reconfiguration of layer 4 connectivity by visual deprivation. Diagram illustrates the circuitry in Control (left) and Deprived (right) layer 4. Deprivation increases the amplitude (thick red axons) and connection probability of excitatory synapses between layer 4 star pyramids. In contrast, the amplitude of inhibitory connections from FS interneurons onto star pyramids was reduced in amplitude (dashed green axons). Finally, inhibitory connections from RSNP neurons onto star pyramids increased in amplitude (thick blue axon) but connection probability was cut in half. These changes should act to boost recurrent excitation within layer 4, while reducing feedback inhibition from FS neurons and leaving feed-forward inhibition roughly constant. (PDF 268 kb)

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