Abstract

Patients with damage to the primary visual cortex (V1) demonstrate residual visual performance during laboratory tasks despite denying having a conscious percept. The mechanisms behind such performance, often called blindsight, are not fully understood, but the use of surgically-induced unilateral V1 lesions in macaque monkeys provides a useful animal model for exploring such mechanisms. For example, V1-lesioned monkeys localize stimuli in a forced-choice condition while at the same time failing to report awareness of identical stimuli in a yes-no detection condition, similar to human patients. Moreover, residual cognitive processes, including saliency-guided eye movements, bottom-up attention with peripheral non-informative cues, and spatial short-term memory, have all been demonstrated in these animals. Here we examined whether post-lesion residual visuomotor processing can be modulated by top-down task knowledge. We tested two V1-lesioned monkeys with a visually guided saccade task in which we provided an informative foveal pre-cue about upcoming target location. Our monkeys fixated while we presented a leftward or rightward arrow (serving as a pre-cue) superimposed on the fixation point (FP). After various cue-target onset asynchronies (CTOAs), a saccadic target (of variable contrast across trials) was presented either in the affected (contra-lesional) or seeing (ipsi-lesional) hemifield. Critically, target location was in the same hemifield that the arrow pre-cue pointed towards in 80% of the trials (valid-cue trials), making the cue highly useful for task performance. In both monkeys, correct saccade reaction times were shorter during valid than invalid trials. Moreover, in one monkey, the ratio of correct saccades towards the affected hemifield was higher during valid than invalid trials. We replicated both reaction time and correct ratio effects in the same monkey using a symbolic color cue. These results suggest that V1-lesion monkeys can use informative cues to localize stimuli in the contra-lesional hemifield, consistent with reports of a human blindsight subject being able to direct attention in cueing paradigms. Because the superior colliculus (SC) may contribute to residual visual capabilities after V1 lesions, and because this structure is important for controlling attentional resources, we hypothesize that our results reflect, among others, SC involvement in integrating top-down task knowledge for guiding orienting behavior.

Highlights

  • Blindsight is a phenomenon that occurs in some patients with damage to their primary visual cortex (V1)

  • By studying the same monkeys as those used in the study of visual awareness mentioned above (Yoshida and Isa, 2015), we have shown that: (1) V1-lesioned monkeys are able to maintain the positions of invisible stimuli in their contra-lesional visual field for as long as 2 s (Takaura et al, 2011); (2) gaze during free-viewing is attracted to invisible but visually salient stimuli in the contra-lesional visual field (Yoshida et al, 2012); and (3) non-informative peripheral pre-cues have a facilitatory effect on visually guided saccades to invisible stimuli in the contralesional visual field (Ikeda et al, 2011)

  • Similar to what we did for psychometric curve thresholds, we examined how the facilitatory effect of the central arrow cue on saccadic reaction time was modulated as a function of cue-target onset asynchronies (CTOAs)

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Summary

Introduction

Blindsight is a phenomenon that occurs in some patients with damage to their primary visual cortex (V1). Blindsight has clinical importance because restoration of visual function, even in the form of blindsight, may improve quality of life in hemianopic patients (Weiskrantz, 2009) Because of this scientific and clinical importance, development of a blindsight animal model is key to expanding our understanding of this condition. One study (Cowey and Stoerig, 1995) has shown that when asked to report the presence or absence of visual stimuli, V1-lesioned monkeys behaved as if they were unaware of the stimuli. These monkeys demonstrated dissociation of visual awareness from forced choice localization, consistent with an objective definition of blindsight. We have identified a behavioral profile in monkeys that resembles blindsight in human subjects who have no visual awareness

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