Three rules govern thalamocortical connectivity of fast-spike inhibitory interneurons in the visual cortex.

Yulia Bereshpolova,Harvey A Swadlow,Xiaojuan Hei,Jose-Manuel Alonso

doi:10.7554/elife.60102

Yulia Bereshpolova, Harvey A Swadlow + Show 2 more

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https://doi.org/10.7554/elife.60102

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Abstract

Some cortical neurons receive highly selective thalamocortical (TC) input, but others do not. Here, we examine connectivity of single thalamic neurons (lateral geniculate nucleus, LGN) onto putative fast-spike inhibitory interneurons in layer 4 of rabbit visual cortex. We show that three 'rules' regulate this connectivity. These rules concern: (1) the precision of retinotopic alignment, (2) the amplitude of the postsynaptic local field potential elicited near the interneuron by spikes of the LGN neuron, and (3) the interneuron's response latency to strong, synchronous LGN input. We found that virtually all first-order fast-spike interneurons receive input from nearly all LGN axons that synapse nearby, regardless of their visual response properties. This was not the case for neighboring regular-spiking neurons. We conclude that profuse and highly promiscuous TC inputs to layer-4 fast-spike inhibitory interneurons generate response properties that are well-suited to mediate a fast, sensitive, and broadly tuned feed-forward inhibition of visual cortical excitatory neurons.

Highlights

Neurons within the visual pathway form highly specific connections to preserve the precise retinotopic organization needed for visual acuity
We studied the functional connectivity between 50 concentric lateral geniculate nucleus (LGN) neurons and 47 layer 4 (L4) SINs (64 LGN-SIN pairs) that had receptive field (RF) aligned, to various extents, with those of the LGN RFs
Once an LGN neuron was isolated and the RF was plotted, a recording electrode was placed in the retinotopically-aligned region of V1

Summary

Introduction

Neurons within the visual pathway form highly specific connections to preserve the precise retinotopic organization needed for visual acuity. Synaptic connectivity between cells of the lateral geniculate nucleus (LGN) and simple cells of the feline visual cortex (V1) is highly dependent on precise retinotopic alignment, and requires a similarity of a number of receptive field (RF) properties of the thalamic inputs and cortical target neurons (Alonso et al, 2001; Hirsch and Martinez, 2006; Sedigh-Sarvestani et al, 2017). A connection probability of ~2/3 is seen between ventrobasal thalamic neurons

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