Identity of a pathway for saccadic suppression

Abstract

Neurons in the superficial gray layer (SGS) of the superior colliculus receive visual input and excite intermediate layer (SGI) neurons that play a critical role in initiating rapid orienting movements of the eyes, called saccades. In the present study, two types of experiments demonstrate that a population of SGI neurons gives rise to a reciprocal pathway that inhibits neurons in SGS. First, in GAD67-GFP knockin mice, GABAergic SGI neurons that expressed GFP fluorescence were injected with the tracer biocytin to reveal their axonal projections. Axons arising from GFP-positive neurons in SGI terminated densely in SGS. Next, SGI neurons in rats and mice were stimulated by using the photolysis of caged glutamate, and in vitro whole-cell patch-clamp recordings were used to measure the responses evoked in SGS cells. Large, synaptically mediated outward currents were evoked in SGS neurons. These currents were blocked by gabazine, confirming that they were GABAA receptor-mediated inhibitory postsynaptic currents. This inhibitory pathway from SGI transiently suppresses visual activity in SGS, which in turn could have multiple effects. These effects could include reduction of perceptual blurring during saccades as well as prevention of eye movements that might be spuriously triggered by the sweep of the visual field across the retina.patch-clamp ͉ photostimulation ͉ sensorimotor ͉ superior colliculus ͉ visuomotor N eurons in the superficial layer (SGS) of the superior colliculus receive input from the retina and the visual cortex (1) and provide a powerful excitatory input to premotor neurons in the intermediate layer (SGI) that play a critical role in initiating rapid orienting movements of the eyes, called saccades (2-4). The activity of many of these superficial layer neurons is suppressed during saccades (5). By reducing the activity in the pathway from the superficial to the premotor cells in the intermediate layer, this suppression may prevent unwanted saccades that might otherwise be triggered by the rapid movement of the visual field that occurs during a saccade. SGS cells also project to nuclei in the dorsal thalamus that relay visual information to the cortex (1), and the reduction of activity in these relay nuclei may contribute to the attenuation of visual perception that occurs during the course of saccades (6-9).Experiments designed to identify the neural mechanisms responsible for saccadic suppression suggest that neither retinal input nor proprioceptive input from the periphery is responsible. For example, superficial layer neurons can respond to visual stimuli moving at the velocity of saccades (5), which suggests that the retinal input is suppressed after reaching SGS. Moreover, the observation that the suppression of activity in SGS can occur during eye movements in the dark indicates that the mechanism is not dependent on changes in the level of retinal activity (5). Similarly, the proposal that the suppression is mediated by input from receptors in extraocular eye muscles or tendons that detect the ...

Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

“…Previous studies have shown that there exist a variety of GABAergic neurons in the SGI, including interlaminar, intralaminar, commissural, and tectofugal projection neurons (Sooksawate et al, 2005;Lee et al, 2007). These various GABAergic neuronal types may have different functional roles in the SC circuitry.…”

“…These various GABAergic neuronal types may have different functional roles in the SC circuitry. For example, a population of interlaminar GABAergic neurons that project to the SGS may inhibit SGS neuronal activity, suppressing unwanted inputs during the course of a saccade (Lee et al, 2007).…”

“…Such a "disinhibition mechanism" has been widely accepted to explain how information from the basal ganglia drives saccades (Wurtz and Hikosaka, 1986;Hikosaka et al, 2006). Recent studies revealed that there are a variety of GABAergic neurons as well as glutamatergic projection neurons in the SGI (Mize, 1992;May, 2005;Sooksawate et al, 2005;Lee et al, 2007), but their functional roles remain essentially unknown. Most of the GABAergic neurons are intra-SC neurons.…”

“…Most of the GABAergic neurons are intra-SC neurons. Their axons mainly project near their somata within SGI, or they innervate the superficial and/or deep layers (Sooksawate et al, 2005;Lee et al, 2007). The simplest and fundamental role of these neurons may be to inhibit local neuronal activity within the SC.…”

Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat

“…The LHAjd, via its bidirectional connections with the SC intermediate and deep layers, has the potential to modulate one or more of these processes; understanding how it may do this will likely require a better understanding of the topographic organization of the multilayered SC. In that regard, one recent study has shed some light on the intrinsic circuitry of the SC (Lee et al, 2007); specifically, it is proposed that the SCig enables saccadic suppression based on the finding of an inhibitory (GABAergic) projection from the SCig to the superficial (retino-recipient) SC layer in rats and mice (Lee et al, 2007). More recently, a PHA-L study of the medial and lateral parts of the SCig identified differences in their projections.…”