Temporal distribution of the ganglion cell volleys in the normal rat optic nerve

Abstract

We describe experiments on behaving rats with electrodes implanted on the cornea, in the optic chiasm, and on the visual cortex; in addition, two red light-emitting diodes (LED) are permanently attached to the skull over the left eye. Recordings timelocked to the LED flashes reveal both the local events at each electrode site and the orderly transfer of visual information from retina to cortex. The major finding is that every stimulus, regardless of its luminance, duration, or the state of retinal light adaptation, elicits an optic nerve volley with a latency of about 10 ms and a duration of about 300 ms. This phenomenon has not been reported previously, so far as we are aware. We conclude that the retina, which originates from the forebrain of the developing embryo, behaves like a typical brain structure: it translates, within a few hundred milliseconds, the chemical information in each pattern of bleached photoreceptors into a corresponding pattern of ganglion cell neuronal information that leaves via the optic nerve. The attributes of each rat ganglion cell appear to include whether the retinal neuropile calls on it to leave after a stimulus and, if so when, within a 300-ms poststimulus epoch. The resulting retinal analysis of the scene, on arrival at the cortical level, is presumed to participate importantly in the creation of visual perceptual experiences.retinal ganglion cells ͉ optic chiasm ͉ visual perception V isual stimuli normally activate the entire retina, as when one drives an automobile or reads text like this. In such situations, saccadic eye movements jerk the eyeballs from one place to the next, coming to rest several times a second with the scene in focus on the retinal surface. To gain further insights into how information is transferred from retina to brain in such situations, we have been studying behaving rats with light-emitting diodes (LED) attached to the skull and electrodes implanted at the anatomical beginning, middle, and end of the visual system. Flashes of light from the LED, which appear to activate the entire retina (1), are varied in duration to simulate natural exposures such as a lightning flash, or the fixation at the end of a saccade, or an attempt to stare at an object without moving the eyes. We present here four simple experiments in which changes in stimulus parameters are correlated with the responses produced throughout the system.Readers will find the data presented here to be only distantly related to the mainstream of current electrophysiological research on animal visual systems. We are not interested in the activities of individual cells in the retinal, thalamic, or cortical neuropiles. We describe instead the activities recordable by large electrodes at three major stations of the system. We emphasize here the retinal neuronal output. We report that ganglion cell axons invariably leave the eyeball in a rigidly predetermined order during about 300 ms, even when the stimuli are delivered at a rate of three Hz. We interpret the data to mean that retinas normally cr...

Sleep modifies retinal ganglion cell responses in the normal rat

“…Our earlier publication presented the evidence for this episodic view of the retinal neuronal output, compared it with the concepts based on conventional microelectrode studies, and suggested a way to reconcile them (1).…”

“…We have reported already that optic nerve axons exit the eyeball in a rigidly prescribed order for about 300 ms after stimulus onset (1). These ganglion cell volleys, called A͞B͞C͞histograms ¶ because of their triphasic waveform, are the inevitable product of rat retinas excited by full-field stimuli, and, we have argued, of human retinas as well.…”

“…Published details (1,2) can be briefly summarized. Young male Wistar rats, under halothane anesthesia and in a stereotaxic device, are implanted with stainless steel electrodes on the cornea, over each visual cortex, and, for sleep-staging, over the parietal cortex.…”

“…e have been studying the visual system of normal, behaving rats stimulated by a light-emitting diode (LED) permanently attached to the skull (1,2). The red LED flashes activate the entire retina from behind the eyeball and evoke responses at electrodes implanted on the corneal surface of the eye, in the optic chiasm, and at the cortical terminal of the pathway.…”

How patterns of bleached rods and cones become visual perceptual experiences: A proposal

“…In an effort to do better with such problems, we have for the past decade been studying rats implanted with both a stimulus-producing device [remotely controlled light-emitting diodes (LED)] and relatively large electrodes that record the retinal and cortical activity the LED stimulation evokes (1,2). The rats are free to move within a small testing box and are studied daily, often for many weeks, when awake and asleep.…”