Abstract
Can direct stimulation of primate V1 substitute for a visual stimulus and mimic its perceptual effect? To address this question, we developed an optical-genetic toolkit to 'read' neural population responses using widefield calcium imaging, while simultaneously using optogenetics to 'write' neural responses into V1 of behaving macaques. We focused on the phenomenon of visual masking, where detection of a dim target is significantly reduced by a co-localized medium-brightness mask (Cornsweet and Pinsker, 1965; Whittle and Swanston, 1974). Using our toolkit, we tested whether V1 optogenetic stimulation can recapitulate the perceptual masking effect of a visual mask. We find that, similar to a visual mask, low-power optostimulation can significantly reduce visual detection sensitivity, that a sublinear interaction between visual- and optogenetic-evoked V1 responses could account for this perceptual effect, and that these neural and behavioral effects are spatially selective. Our toolkit and results open the door for further exploration of perceptual substitutions by direct stimulation of sensory cortex.
Highlights
A central goal of sensory neuroscience, and a prerequisite for the development of effective sensory cortical neuroprostheses, is to understand the nature of the neural code – that is, to determine which patterns of neural activity in early sensory cortex are necessary and sufficient to elicit a given percept
The overarching goal of the current study was to test two related hypotheses: (i) that low-power optogenetic stimulation can substitute for a localized visual mask and cause a significant drop in behavioral detection sensitivities, and (ii) that this perceptual effect is caused by a sublinear interaction between the neural responses elicited in macaque visual cortex (V1) by simultaneous visual and direct optogenetic stimulation
We developed an optical-genetic toolkit that allowed us to simultaneously measure and stimulate optically neural responses in the cortex of behaving macaques
Summary
A central goal of sensory neuroscience, and a prerequisite for the development of effective sensory cortical neuroprostheses, is to understand the nature of the neural code – that is, to determine which patterns of neural activity in early sensory cortex are necessary and sufficient to elicit a given percept. By carefully monitoring behavior while animals perform demanding sensory tasks, the perceptual consequences of these 42 inserted signals can be assessed and compared with theoretical predictions. This powerful experimental approach for all-optical interrogation of sensory cortex has recently been successfully used to study the neural code in rodents (e.g., [3,4,5]). The merging of optostim and optical imaging of calcium signals in behaving non-human primates (NHPs), an important animal model for studying human perception, is still in its infancy [6], and simultaneous imaging, optogenetic stimulation and behavior have not been achieved previously in NHPs. Multiple barriers remain before this approach can be used routinely in NHPs [7,8,9]. While optostim in early sensory cortex has been demonstrated to cause clear neural (e.g., [6, 10,11,12,13,14]) and behavioral (e.g., [6, 12,13,14]) effects in NHPs, such experiments typically require high-power optostimulation (10s to 100s of mW/mm2), and the evoked neural responses are typically monitored by electrophysiology which only captures a small fraction of the optostim-triggered neural population response
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