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.
A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex
