The foveal visual representation of the primate superior colliculus

Abstract

13Processing of foveal retinal input is important not only for high quality visual scene analysis, but 14 also for ensuring precise, albeit tiny, gaze shifts during high acuity visual tasks. The 15 representations of foveal retinal input in primate lateral geniculate nucleus and early visual 16 cortices have been characterized. However, how such representations translate into precise eye 17 movements remains unclear. Here we document functional and structural properties of the foveal 18 visual representation of midbrain superior colliculus. We show that superior colliculus, 19 classically associated with extra-foveal spatial representations needed for gaze shifts, is highly 20 sensitive to visual input impinging on the fovea. Superior colliculus also represents such input in 21 an orderly and very specific manner, and it magnifies representation of foveal images in neural 22 tissue as much as primary visual cortex does. Primate superior colliculus contains a high-fidelity 23 visual representation, with large foveal magnification, perfectly suited for active visuomotor 24 control and perception. 25 26 27 94 Figure 1 Foveal visual neurons of primate superior colliculus (SC). (A) Four example neurons recorded from right 95 SC in awake monkeys. Top: visual response fields (RF's) in polar coordinates (Materials and Methods). Middle: same 96 RF's using log-polar coordinates magnifying small eccentricities (15). Bottom: raw firing rates (blue) along with 97 s.e.m. error bars (dashed blue) when a stimulus was presented near the neuron's RF hotspot (Materials and Methods). 98 Individual rasters show raw spike (action potential) times across repetitions of stimulus presentation. All neurons had 99 RF's almost entirely contained within the rod-sparse foveola region (i.e. <0.5 deg eccentricity; (6-8)). Different 100 neurons tiled different portions of foveal space (top two rows), and all had strong sensitivity. (B) Across both right 101 and left SC's, the entire foveal space was represented. Each small circle indicates RF hotspot location from an example 102 neuron, and solid lines indicate RF inner boundaries. (C) Foveal RF's were much smaller than peripheral ones. Six 103 example neurons with RF boundaries and hotspot locations indicated by outlines and small circles, respectively. Right: 104 log-polar coordinates magnifying the small, but highly well-defined visual RF's of the foveal neurons. Also see Fig. 105 2A. 106 107 Strong visual sensitivity was additionally reflected in neural response latency (29-31): 108first-spike latency (Materials and Methods) was similar to that in peripheral neurons (Fig. S2C). 109 Only in superficial SC layers, response latency decreased with increasing eccentricity within the 110 central 2 deg (Fig. S2C, blue). Because superficial neurons, but not deeper ones, receive direct 111 retinal input (3-5), this non-uniformity could reflect the sparseness of rod photoreceptors (having 112 fast integration times) in foveola. 113 130 microsaccades are needed to re-align gaze (16): tiny microsa...

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

“…We asked two monkeys (P and N) to maintain steady fixation on a central spot. Prior work has shown that this condition gives rise to frequent microsaccades, which are associated with movement-related bursts in the rostral region of the SC representing small visual eccentricities and movement vectors (Hafed et al, 2009; Hafed and Krauzlis, 2012; Chen et al, 2019; Willeke et al, 2019). In experiments 1 and 2, we then presented a visual stimulus at a more eccentric location, and we recorded neural activity at this location (Fig.…”

“…We first tested the hypothesis that visually-induced action potentials can occur in the SC intra-saccadically; that is, putatively simultaneously with motor-related bursts. We exploited the topographic nature of the SC in representing visual and motor space (Cynader and Berman, 1972; Robinson, 1972; Chen et al, 2019). We asked two monkeys (P and N) to maintain steady fixation on a central spot.…”

Saccades along spatial neural circuit discontinuities

“…However, again here, it is surprisingly hard to find literature on detailed individual RF mappings near the vertical and horizontal meridians. Based on our own experience, we find that RF's near the vertical meridian seem to still have preference for the contralateral side even when their RF's extend spatially in the ipsilateral hemifield (Chen et al 2019;Hafed and Chen 2016). That is, the RF hotspot location is still lateralized even when the RF extent does cross the vertical meridian discontinuity.…”

“…For example, in the SC, it is thought that the locus of activity on the SC map defines the desired saccade amplitude and direction (Cynader and Berman 1972;Lee et al 1988;Robinson 1972;van Opstal et al 1991;Wurtz and Goldberg 1972a;1971). Thus, the anatomical location of a neuron dictates the vector that it represents, resulting in a topographic map (Chen et al 2019;Cynader and Berman 1972;Hafed and Chen 2016;Robinson 1972). However, due to lateralization, there is a structural discontinuity in this map, with the visual field being divided along the vertical meridian into a left and right SC representation.…”

“…Historically, it was suggested that representations near the vertical meridian in the SC (and other sensory and sensory-motor structures) are bilateral, thus allowing coding of purely vertical saccades (Baizer et al 1991;Dow et al 1981;Goldberg and Wurtz 1972;Hafed and Chen 2016;Hafed et al 2009;Leicester 1968;Pigarev et al 2001;Schneider et al 2004;Updyke 1974). However, there still seems to be a contralateral preference in SC neurons' response field (RF) hotspot locations, with only the RF boundaries extending to cross into the ipsilateral side (Chen et al 2019;Cowey and Perry 1980;Goldberg and Wurtz 1972;Hafed and Chen 2016;Updyke 1974). As a result, it may be asked whether there are ever purely vertical saccades (and similarly for horizontal movements) when there may never be purely vertical (or horizontal) RF hotspot locations in structures like the SC.…”