Stimulus-dependent correlated firing in directionally selective retinal ganglion cells

Abstract

Synchronous spiking has been postulated to be a meta-signal in visual cortex and other CNS loci that tags neuronal spike responses to a single entity. In retina, however, synchronized spikes have been postulated to arise via mechanisms that would largely preclude their carrying such a code. One such mechanism is gap junction coupling, in which synchronous spikes would be a by-product of lateral signal sharing. Synchronous spikes have also been postulated to arise from common-source inputs to retinal ganglion cells having overlapping receptive fields, and thus code for stimulus location in the overlap area. On–Off directionally selective ganglion cells of the rabbit retina exhibit a highly precise tiling pattern in which gap junction coupling occurs between some neighboring, same-preferred-direction cells. Depending on how correlated spikes arise, and for what purpose, one could postulate that synchronized spikes in this system (1) always arise in some subset of same-direction cells because of gap junctions, but never in non-same-preferred-directional cells; (2) never arise in same-directional cells because their receptive fields do not overlap, but arise only in different-directional cells whose receptive fields overlap, as a code for location in the overlap region; or (3) arise in a stimulus-dependent manner for both same- and different-preferred-direction cells for a function similar to that postulated for neurons in visual cortex. Simultaneous, extracellular recordings were obtained from neighboring On–Off directionally selective (DS) ganglion cells having the same and different preferred directions in an isolated rabbit retinal preparation. Stimulation by large flashing spots elicited responses from DS ganglion-cell pairs that typically showed little synchronous firing. Movement of extended bars, however, often produced synchronous spikes in cells having similar or orthogonal preferred directions. Surprisingly, correlated firing could occur for the opposite contrast polarity edges of moving stimuli when the leading edge of a sweeping bar excited the receptive field of one cell as its trailing edge stimulated another. Pharmacological manipulations showed that the spike synchronization is enhanced by excitatory cholinergic amacrine-cell inputs, and reduced by inhibitory GABAergic inputs, in a motion-specific manner. One possible interpretation is that this synchronous firing could be a signal to higher centers that the outputs of the two DS ganglion cells should be “bound” together as responding to a contour of a common object.