Efficacy of Retinal Spikes in Driving Cortical Responses

How does a single retinal ganglion cell (RGC) affect the firing of simple cells in the visual cortex? Although much is known of the functional connections between the retina and the lateral geniculate nucleus (LGN) and between LGN and visual cortex, it is hard to infer the effect of disynaptic connections from retina to visual cortex. Most importantly, there is considerable divergence from retina to LGN, so cortical neurons might be influenced by ganglion cells through multiple feedforward pathways. We recorded simultaneously from ganglion cells in the retina and cortical simple cells in the striate cortex with overlapping receptive fields and evaluated disynaptic connections with cross-correlation analysis. In all disynaptically connected pairs, the retinal receptive field center and overlapping cortical subregion always shared the same sign (either both ON or both OFF). Connected pairs were similar in other respects, such as relative position and timing of their receptive fields, and thus obeyed the same rules of connectivity found previously for retinothalamic and thalamocortical connections. We found that a single RGC directly contributed on average to ∼3% of the activity of its cortical target. The relative timing of pairs of spikes from the retinal cell affected their efficacy in driving the cortical cell. When two retinal spikes were closely spaced (<10 msec), the second spike was several times more likely to drive the cortical target. The relative magnitude of this disynaptic paired spike enhancement was considerably larger than has been found previously for retinogeniculate and geniculocortical connections. The amplified paired spike enhancement from retina to cortex ensures that signal transmission from retina to cortex is particularly effective when the retina fires a series of closely spaced action potentials.