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Direction selectivity in the retina: symmetry and asymmetry in structure and function

This article has been updated

Key Points

  • Direction-selective retinal ganglions cells (DSGCs) consist of several distinct types that branch at different levels in the inner retina. Most types are comprised of multiple subtypes, each of which responds to image motion in a different preferred direction. Recent studies have identified specific molecular markers that are expressed either endogenously or transgenically by particular subtypes of DSGC.

  • In most cases, the key player in the generation of direction selectivity in the retina is the starburst amacrine cell (SAC), which is a morphologically symmetrical interneuron that contains both GABA and acetylcholine (ACh). The release of GABA from individual distal dendrites of SACs is itself direction selective, owing to the sequential activation of excitatory inputs along the dendrite together with intrinsic nonlinearities in the SAC; inhibitory interactions between overlapping SACs also seem to have a role.

  • The directional output from individual dendrites is preserved because dendrites on different sides of the SAC make selective inhibitory synapses on different subtypes of DSGCs, thus establishing their preferred direction. The centrifugal separation of input and output synapses along the SAC dendrites provides the fundamental spatial asymmetry that underlies the generation of direction selectivity in the retina.

  • The asymmetric GABAergic inhibition from SACs interacts with symmetric cholinergic excitation from SACs and glutamatergic excitation from bipolar cells within local regions of the DSGC's dendritic tree. The summed inputs within each of these functional subunits are locally thresholded, producing dendritic spikes that propagate to the soma independently of the activity in other subunits.

  • The development of the different subtypes of DSGCs and their selective connectivity with the SACs seems to be mainly governed by intrinsic mechanisms, with visual stimulation and spontaneous neuronal activity playing negligible roles.

Abstract

Visual information is processed in the retina to a remarkable degree before it is transmitted to higher visual centres. Several types of retinal ganglion cells (the output neurons of the retina) respond preferentially to image motion in a particular direction, and each type of direction-selective ganglion cell (DSGC) is comprised of multiple subtypes with different preferred directions. The direction selectivity of the cells is generated by diverse mechanisms operating within microcircuits that rely on independent neuronal processing in individual dendrites of both the DSGCs and the presynaptic neurons that innervate them.

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Figure 1: Neuronal organization of the retina.
Figure 2: Dendritic morphology and receptive-field properties of direction-selective ganglion cells.
Figure 3: Cellular mosaics of direction-selective ganglion cells.
Figure 4: Synaptic connectivity between starburst amacrine cells and On–Off direction-selective ganglion cells.
Figure 5: Direction-selective responses in starburst amacrine cells.
Figure 6: Circuit diagram of direction selectivity in the retina.

Change history

  • 10 February 2012

    In the reference list of this article, the text underneath reference 86 should have been placed under reference 87 and should have referred to reference 79, rather than reference 78. This has now been corrected in the online pdf.

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Acknowledgements

This paper is dedicated to Horace Barlow on the occasion of his ninetieth birthday and Bill Levick on the occasion of his eightieth birthday, in recognition of their outstanding pioneering studies on direction selectivity in the retina, which laid the foundation for the research described in this Review. W.R.T. is supported by a grant from the National Eye Institute (EY014888) and a Lew R. Wasserman Award from Research to Prevent Blindness.

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Glossary

Microcircuit

An assembly of neural elements that are smaller than whole neurons but can independently perform computations.

Accessory optic system

(AOS). The AOS is the fourth primary visual system, after the thalamic, tectal and pretectal systems, and comprises the medial, lateral and dorsal terminal nuclei.

Varicosities

Swellings along neuronal processes that are the sites of en passant synapses.

Channelrhodopsin 2

A light-gated ion channel that can be genetically expressed in individual neurons or populations of neurons, enabling them to be depolarized selectively by photostimulation.

Serial block-face scanning electron microscopy

A technique for obtaining unbroken aligned series of images at sub-micron resolution by successively scanning then sectioning the face of the specimen block on the same apparatus.

Reversal potential

The membrane potential at which the net ion current flow becomes zero.

Inhibitory shunt

Suppression of excitatory postsynaptic potentials resulting from an increase in neuronal membrane conductance.

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Vaney, D., Sivyer, B. & Taylor, W. Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci 13, 194–208 (2012). https://doi.org/10.1038/nrn3165

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