Image-dependence of the detectability of optogenetic stimulation in macaque inferotemporal cortex

Artificial activation of neurons in early visual areas induces perception of simple visual flashes.1Brindley G.S. Lewin W.S. The sensations produced by electrical stimulation of the visual cortex.J. Physiol. 1968; 196: 479-493https://doi.org/10.1113/jphysiol.1968.sp008519Crossref PubMed Scopus (849) Google Scholar,2Murphey D.K. Maunsell J.H.R. Beauchamp M.S. Yoshor D. Perceiving electrical stimulation of identified human visual areas.Proc. Natl. Acad. Sci. USA. 2009; 106: 5389-5393https://doi.org/10.1073/pnas.0804998106Crossref PubMed Scopus (88) Google Scholar Accordingly, stimulation in high-level visual cortices is expected to induce perception of complex features.3Gross C.G. De Schonen S. Representation of Visual Stimuli in Inferior Temporal Cortex [and Discussion].Philos. Trans. R. Soc. Lond. B Biol. Sci. 1992; 335: 3-10Crossref PubMed Scopus (204) Google Scholar,4Kanwisher N. McDermott J. Chun M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception.J. Neurosci. 1997; 17: 4302-4311https://doi.org/10.1523/JNEUROSCI.17-11-04302.1997Crossref PubMed Google Scholar However, results from studies in human patients challenge this expectation. Stimulation rarely induces any detectable visual event, and never a complex one, in human subjects with closed eyes.2Murphey D.K. Maunsell J.H.R. Beauchamp M.S. Yoshor D. Perceiving electrical stimulation of identified human visual areas.Proc. Natl. Acad. Sci. USA. 2009; 106: 5389-5393https://doi.org/10.1073/pnas.0804998106Crossref PubMed Scopus (88) Google Scholar Stimulation of the face-selective cortex in a human patient led to remarkable hallucinations only while the subject was looking at faces.5Parvizi J. Jacques C. Foster B.L. Witthoft N. Rangarajan V. Weiner K.S. Grill-Spector K. Electrical stimulation of human fusiform face-selective regions distorts face perception.J. Neurosci. 2012; 32: 14915-14920https://doi.org/10.1523/JNEUROSCI.2609-12.2012Crossref PubMed Scopus (238) Google Scholar In contrast, stimulations of color- and face-selective sites evoke notable hallucinations independent of the object being viewed.6Schalk G. Kapeller C. Guger C. Ogawa H. Hiroshima S. Lafer-Sousa R. Saygin Z.M. Kamada K. Kanwisher N. Facephenes and rainbows: Causal evidence for functional and anatomical specificity of face and color processing in the human brain.Proc. Natl. Acad. Sci. USA. 2017; 114: 12285-12290https://doi.org/10.1073/pnas.1713447114Crossref PubMed Scopus (66) Google Scholar These anecdotal observations suggest that stimulation of high-level visual cortex can evoke perception of complex visual features, but these effects depend on the availability and content of visual input. In this study, we introduce a novel psychophysical task to systematically investigate characteristics of the perceptual events evoked by optogenetic stimulation of macaque inferior temporal (IT) cortex. We trained macaque monkeys to detect and report optogenetic impulses delivered to their IT cortices7Murphey D.K. Maunsell J.H.R. Behavioral detection of electrical microstimulation in different cortical visual areas.Curr. Biol. 2007; 17: 862-867https://doi.org/10.1016/j.cub.2007.03.066Abstract Full Text Full Text PDF PubMed Scopus (82) Google Scholar,8May T. Ozden I. Brush B. Borton D. Wagner F. Agha N. Sheinberg D.L. Nurmikko A.V. Detection of optogenetic stimulation in somatosensory cortex by non-human primates--towards artificial tactile sensation.PLoS One. 2014; 9: e114529https://doi.org/10.1371/journal.pone.0114529Crossref PubMed Scopus (36) Google Scholar,9Dai J. Brooks D.I. Sheinberg D.L. Optogenetic and electrical microstimulation systematically bias visuospatial choice in primates.Curr. Biol. 2014; 24: 63-69https://doi.org/10.1016/j.cub.2013.11.011Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar while holding fixation on object images. In a series of experiments, we show that detection of cortical stimulation is highly dependent on the choice of images presented to the eyes and it is most difficult when fixating on a blank screen. These findings suggest that optogenetic stimulation of high-level visual cortex results in easily detectable distortions of the concurrent contents of vision.