Visual Responses of Ganglion Cells

Ralph Nelson

[Overview] [History of Electrical Recordings] [ON and OFF Responses] [Receptive field] [Centers and Surrounds] [Contrast Sensitivity functions and Difference of Gaussians] [X and Y receptive fields] [Directionally Selective Ganglion Cells] [Modeling Directional Selectivity] [Pharmacology of Directional Selectivity] [Color and Spectral Responses] [Color and Receptive Fields] [Tonic and phasic ganglion cells of primate retina] [Color properties of primate ganglion cells] [Rod signals in retinal ganglion cells] [Rod signals are delayed] [Detection of light quanta by retinal ganglion cells] [Receptive field alterations with rod vision] [Spatial distribution of ganglion cell fields] [Ganglion cell mosaics and spatial resolution] [Correlated firing of neighboring ganglion cells] [Neurotransmitter receptors and synaptic currents] [Ganglion cells that are involved in the circadian clock] [References]

1. Overview.

Ganglion cells are the final output neurons of the vertebrate retina. Ganglion cells collect information about the visual world from bipolar cells and amacrine cells (retinal interneurons). This information is in the form of chemical messages sensed by receptors on the ganglion cell membrane. Transmembrane receptors, in turn, transform the chemical messages into intracellular electrical signals. These are integrated within ganglion-cell dendrites and cell body, and 'digitized', probably in the initial segment of the ganglion-cell axon, into nerve spikes. Nerve spikes are a time-coded digital form of electrical signalling used to transmit nervous system information over long distances, in this case through the optic nerve and into brain visual centers.

Ganglion cells are also the most complex information processing systems in the vertebrate retina. It is a general experimental truth that an organism as a whole cannot behaviorally respond to visual stimuli that are not also detectable by individual ganglion cells. Different cells become selectively tuned to detect surprisingly subtle 'features' of the visual scene, including color, size, and direction and speed of motion. These are called 'trigger features'. Even so signals detected by ganglion cells may not have a unique interpretation. Equivalent signals might result from an object changing brightness, changing shape, or moving. It is up to the brain to determine the most likely interpretation of detected events and, in the context of events detected by other ganglion cells, take appropriate action.

Ganglion cell axons terminate in brain visual centers, principally the lateral geniculate nucleus and the superior colliculus. Ganglion cell axons are directed to specific visual centers depending on the visual 'trigger features' they encode. The optic nerve collects all the axons of the ganglion cells. In man this optic nerve bundle contains more than a million axons.

2. History of Electrical Recordings.

In 1967 Ragnar Granit and H. Keffer Hartline shared the Nobel prize in physiology and medicine for the first electrical recordings of light responses from individual ganglion cells of the vertebrate retina. In this, both laureates acknowledged the earlier seminal influence of Edgar D. Adrian, winner of the 1932 Nobel prize in physiology and medicine. Adrian pioneered the measurement of impulse discharges from individual peripheral nerve axons and was principally responsible for the discovery that nerve fibers transmit signals in the form of a temporal sequence of 'all or none' impulses. Granit also noted the influence of the anatomist Santiago Ramon y Cajal, winner of the 1906 Nobel prize, in illustrating a complex retinal circuitry worthy of physiological investigation.

Hartline pushed experimental technology of the 1930's to its limits in obtaining extracellular recordings of individual ganglion cells. There were no solid state electronics. Special purpose, 'direct coupled' vacuum tube amplifiers were designed. There were no oscilloscopes or computers for display and storage of signals. String galvanometers were used; a pencil of light played from a tiny mirror, minutely vibrating in a magnetic field, onto moving photographic film to document electrical events. There were no microelectrodes; ganglion cell axon bundles were teased off the retinal surface with dissecting tools and lifted onto a course cotton wick electrode, such as earlier used for massed potential recordings. Ultimately this technique proved too difficult to pursue and left no legacy. It remained for Granit (1947) to introduce microelectrodes for such recordings, which greatly facilitated the ease of data collection. Granit also made the first ganglion cell recordings from a mammalian retina, the cat retina. This retina, as pursued by his students and others, has been a staple of visual electrophysiology. Yet the experimental designs and approaches provided by Hartline continue to be used. So many of his findings, such as the multiplicity of ganglion cell response types, have proved accurate, such that the succeeding field of ganglion cell electrophysiology sometimes appears almost as a footnote to his work.

Fig. 1.Haldan Keffer Hartline, 1967 Nobel Laureate..

Fig. 2. Ragnar Granit, 1967 Nobel Laureate.

3. ON and OFF Responses.

Hartline's electrical recordings of single optic nerve fiber responses revealed 'discharges of impulses', or 'action potentials' in response to light stimulation. The discharge patterns were, however, diverse (Hartline, 1938). Three unique patterns of light response were described (Fig.3).

Fig. 3. ON, OFF and ON-OFF ganglion cells. From Hartline (1938; 1967).

Fig. 4. Stratification of ON and Off center Ganglion cells within the inner plexiform layer. From Nelson et al. (1978).