Adaptation to Binocular Anticorrelation Results in Increased Neural Excitability

Abstract

Abstract Throughout the brain, information from individual sources converges onto higher order neurons. For example, information from the two eyes first converges in binocular neurons in area V1. Some neurons are tuned to similarities between sources of information, which makes intuitive sense in a system striving to match multiple sensory signals to a single external cause—that is, establish causal inference. However, there are also neurons that are tuned to dissimilar information. In particular, some binocular neurons respond maximally to a dark feature in one eye and a light feature in the other. Despite compelling neurophysiological and behavioral evidence supporting the existence of these neurons [Katyal, S., Vergeer, M., He, S., He, B., & Engel, S. A. Conflict-sensitive neurons gate interocular suppression in human visual cortex. Scientific Reports, 8, 1239, 2018; Kingdom, F. A. A., Jennings, B. J., & Georgeson, M. A. Adaptation to interocular difference. Journal of Vision, 18, 9, 2018; Janssen, P., Vogels, R., Liu, Y., & Orban, G. A. At least at the level of inferior temporal cortex, the stereo correspondence problem is solved. Neuron, 37, 693–701, 2003; Tsao, D. Y., Conway, B. R., & Livingstone, M. S. Receptive fields of disparity-tuned simple cells in macaque V1. Neuron, 38, 103–114, 2003; Cumming, B. G., & Parker, A. J. Responses of primary visual cortical neurons to binocular disparity without depth perception. Nature, 389, 280–283, 1997], their function has remained opaque. To determine how neural mechanisms tuned to dissimilarities support perception, here we use electroencephalography to measure human observers' steady-state visually evoked potentials in response to change in depth after prolonged viewing of anticorrelated and correlated random-dot stereograms (RDS). We find that adaptation to anticorrelated RDS results in larger steady-state visually evoked potentials, whereas adaptation to correlated RDS has no effect. These results are consistent with recent theoretical work suggesting “what not” neurons play a suppressive role in supporting stereopsis [Goncalves, N. R., & Welchman, A. E. “What not” detectors help the brain see in depth. Current Biology, 27, 1403–1412, 2017]; that is, selective adaptation of neurons tuned to binocular mismatches reduces suppression resulting in increased neural excitability.