Direction-Selective Ganglion Cells in the Retina

Abstract

The first stages in the neuronal processing of image motion take place within the retina. Some types of ganglion cells, which are the output neurones of the retina, are strongly stimulated by image movement in one direction, but are inhibited by movement in the opposite direction. Such direction selectivity represents an early level of complex visual processing which has been intensively studied from morphological, physiological, pharmacological and theoretical perspectives. Although this computation is performed within two or three synapses of the sensory input, the cellular locus and the synaptic mechanisms of direction selectivity have yet to be elucidated.

The classic study by Barlow and Levick (1965) characterized the receptive-field properties of direction-selective (DS) ganglion cells in the rabbit retina and established that there are both inhibitory and facilitatory mechanisms underlying the direction selectivity. In each part (“subunit”) of the receptive field, apparent-motion experiments indicated that a spatially asymmetric, delayed or long-lasting inhibition “vetoes” excitation for movement in one direction (the “null” direction), but not for movement in the opposite direction (the “preferred” direction). In addition, facilitation of excitatory inputs occurs for movement in the preferred direction.

Subsequently, pharmacological experiments indicated that a GABAergic input from lateral association neurones (amacrine cells) may inhibit an excitatory cholinergic input from other amacrine cells and/or a glutamatergic input from second-order intemeurones (bipolar cells). An added complication is that the cholinergic amacrine cells also synthesize and contain GABA, raising the possibility that these “starburst” cells mediate both the excitation and inhibition underlying direction selectivity (Vaney et al. 1989).

This review focuses on recent studies that shed light on the cellular mechanisms that underlie direction selectivity in retinal ganglion cells. He and Masland (1997) have provided compelling evidence that the cholinergic amacrine cells mediate the facilitation elicited by motion in the preferred direction; however, it now appears that the cholinergic facilitation is non-directional, although the null-direction facilitation is normally masked by the directional inhibitory mechanism. The null-direction inhibition may act presynaptically on the excitatory input to the DS ganglion cell; in this case, the release of transmitter from the excitatory neurone would itself be direction selective, at least locally. Alternatively, the null-direction inhibition may act postsynaptically on the ganglion cell dendrites, probably through the non-linear mechanism of shunting inhibition.

In the rabbit retina, there are two distinct types of DS ganglion cells which respond with either On-Off or On responses to flashed illumination; the two types also differ in their specificity for stimulus size and speed and their central projections. The On-Off DS cells comprise four physiological subtypes, whose preferred directions are aligned with the horizontal and vertical ocular axes, whereas the On DS cells comprise three physiological subtypes, whose preferred directions correspond to rotation about the best response axes of the three semicircular canals in the inner ear. The On DS cells, which project to the accessory optic system, appear to respond to global slippage of the retinal image, thus providing a signal that drives the optokinetic reflex. The On-Off DS cells, which are about ten times more numerous than the On DS cells, appear to signal local motion and they may playa key role in the representation of dynamic visual space or the detection of moving objects in the environment.