Stimulus size dependence of information transfer from retina to thalamus

Robert Uglesich

doi:10.3389/neuro.06.010.2009

Abstract

Relay cells in the mammalian lateral geniculate nucleus (LGN) are driven primarily by single retinal ganglion cells (RGCs). However, an LGN cell responds typically to less than half of the spikes it receives from the RGC that drives it, and without retinal drive the LGN is silent (Kaplan and Shapley, 1984). Recent studies, which used stimuli restricted to the receptive field (RF) center, show that despite the great loss of spikes, more than half of the information carried by the RGC discharge is typically preserved in the LGN discharge (Sincich et al., 2009), suggesting that the retinal spikes that are deleted by the LGN carry less information than those that are transmitted to the cortex. To determine how LGN relay neurons decide which retinal spikes to respond to, we recorded extracellularly from the cat LGN relay cell spikes together with the slow synaptic (‘S’) potentials that signal the firing of retinal spikes. We investigated the influence of the inhibitory surround of the LGN RF by stimulating the eyes with spots of various sizes, the largest of which covered the center and surround of the LGN relay cell's RF. We found that for stimuli that activated mostly the RF center, each LGN spike delivered more information than the retinal spike, but this difference was reduced as stimulus size increased to cover the RF surround. To evaluate the optimality of the LGN editing of retinal spikes, we created artificial spike trains from the retinal ones by various deletion schemes. We found that single LGN cells transmitted less information than an optimal detector could.

Highlights

All we know about patterns and objects in the visual world comes to us courtesy of the discharge of the relay neurons of the lateral geniculate nucleus (LGN), which convey the retinal messages to the visual cortex
DOES THE ENHANCED SURROUND OF LGN RECEPTIVE FIELDS PLAY A ROLE IN INFORMATION TRANSMISSION? It had been reported previously (Hubel and Wiesel, 1961; Maffei et al, 1970; Dubin and Cleland, 1977; So and Shapley, 1981; Kaplan et al, 1993) that compared to the RFs of RGCs, the stronger surround of LGN RFs attenuates primarily low spatial and temporal frequencies, which makes the LGN cell more sharply tuned than the RGC that drives it. One might expect this improved filtering to help in communicating retinal information to the visual cortex, but our results show that as stimulus size grows, information rate does not
We found that upon going from small to large spot sizes, the time averaged coefficient of variation changed little (≤6%) for the RGCs, but increased by 30% for the LGN

Summary

Introduction

All we know about patterns and objects in the visual world comes to us courtesy of the discharge of the relay neurons of the lateral geniculate nucleus (LGN), which convey the retinal messages to the visual cortex. On average, the LGN fires only four spikes for every 10 spikes that the retina delivers to it. We know that all LGN impulses are elicited by retinal spikes (Kaplan and Shapley, 1984), and the LGN can only delete spikes from the incoming retinal message. These observations suggest that, if an LGN cell is to avoid losing much of the information delivered to it by the retina, it must select the most informative spikes for transmission, and block or ignore the less informative spikes, and it must do so across a wide range of stimulus types and sizes. The impact of the inhibitory surround on the cell’s sensitivity and response becomes important for both retina and especially the LGN (Hubel and Wiesel, 1961)

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