Sleep modifies retinal ganglion cell responses in the normal rat

Abstract

Recordings were obtained from the visual system of rats as they cycled normally between waking (W), slow-wave sleep (SWS), and rapid eye movement (REM) sleep. Responses to flashes delivered by a light-emitting diode attached permanently to the skull were recorded through electrodes implanted on the cornea, in the chiasm, and on the cortex. The chiasm response reveals the temporal order in which the activated ganglion cell population exits the eyeball; as reported, this triphasic event is invariably short in latency (5-10 ms) and around 300 ms in duration, called the histogram. Here we describe the differences in the histograms recorded during W, SWS, and REM. SWS histograms are always larger than W histograms, and an REM histogram can resemble either. In other words, the optic nerve response to a given stimulus is labile; its configuration depends on whether the rat is asleep or awake. We link this physiological information with the anatomical fact that the brain dorsal raphe region, which is known to have a sleep regulatory role, sends fibers to the rat retina and receives fibers from it. At the cortical electrode, the visual cortical response amplitudes also vary, being largest during SWS. This well known phenomenon often is explained by changes taking place at the thalamic level. However, in the rat, the labile cortical response covaries with the labile optic nerve response, which suggests the cortical response enhancement during SWS is determined more by what happens in the retina than by what happens in the thalamus.optic chiasm ͉ 5-HT ͉ efferent retinal innervation W 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. The overall objective is to describe the ganglion cell volley the retina creates as it converts rod͞cone photochemical information into its neuronal equivalents and to follow that neuronal activity as it moves past the chiasm electrode en route, mainly, to the lateral geniculate nucleus (LGN) and the cortex beyond.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. Here we compare the histograms of sleeping and waking (W) rats, show they are labile, and conclude that optic nerve modulation probably is controlled by the serotonin fibers known to reach the retina from the midbrain dorsal raphe nuclei. Finally, we show that the well known cortical response enhancement during SWS is the approximate mirror image of the enhanced ganglion cell histogram, and we discuss the significance of this fact. ...

Serotonergic Retinopetal Axons in the Monkey Retina

“…Changes in the activity of retinal ganglion cells in rats during sleep have been attributed to serotonergic retinopetal axons. 32 Acting through 5-HT 2 receptors, serotonin reduces the current through GABA C receptors of rod bipolar cells in rats 33 and also inhibits the release of thyrotropin releasing hormone from rat retinas. 34 In cat retinas, 5-HT decreases the maintained firing rates of ON center ganglion cells and increases the rates of OFF center cells.…”

Cumulative latency advance underlies fast visual processing in desynchronized brain state

“…Similar to V1 neurons, the elevated membrane potential and shortened membrane time constant caused by the conductance increase can both contribute to the latency advance of LGN neurons. Furthermore, retinal ganglion cell responses in rat can be modulated by brain state, possibly mediated by the serotonin input to the retina from the dorsal raphe (37). Therefore, retinal ganglion cells may also exhibit brain state-dependent latency advance, which can contribute to that of LGN neurons.…”

Using the Electroretinogram to Assess Function in the Rodent Retina and the Protective Effects of Remote Limb Ischemic Preconditioning

“…Neuromuscular blockers and anaesthetic agents are used in ERG experimentation to achieve an unconscious and motionless state. There have only been five reports of awake ERG recordings in rats [16][17][18][19][20] . In these studies, electrodes were surgically pre-implanted into the skull and two of these studies tested the effect of anaesthesia on the ERG 17,20 .…”