Retinal direction of motion is reliably transmitted to visual cortex through highly selective thalamocortical connections.

Abstract

Motion perception is crucial to animal survival and effective environmental interactions. In mammals, detection of movement begins in the retina. Directionally selective (DS) retinal ganglion cells were first discovered in the rabbit eye,¹ and they have since been found in mouse,^2,3 cat,⁴ and monkey.^5,6 These DS retinal neurons contact a small population of neurons in the visual thalamus (dorsal lateral geniculate nucleus [LGN]) that are highly DS.^7,8,9,10 The primary visual cortex (V1) also contains DS neurons, but whether directional selectivity in V1 emerges de novo^11,12,13 or is inherited from DS thalamic inputs^14,15,16 remains unclear. We previously found that LGN-DS neurons generate strong and focal synaptic currents in rabbit V1, similar to those generated by LGN concentric cells.¹⁷ Thus, the synaptic drive generated by LGN-DS neurons in V1 is spatially well situated to influence the firing of layer 4 (L4) simple cells, most of which show strong directional selectivity.¹⁸ However, two important questions remain: do LGN-DS neurons synaptically target DS simple cells in L4, and, if so, do they contribute to the directional preferences of these V1 DS neurons? We used spike-train cross-correlation analysis of pairs of LGN-DS and L4 simple cells to address these questions. We found that LGN-DS neurons do target L4 DS simple cells and that the targeting is highly selective, largely following a simple set of "connectivity rules." We conclude that this highly selective thalamocortical connectivity of LGN-DS neurons contributes to the sharp directional selectivity of cortical simple cells.