Neocortical Rebound Depolarization Enhances Visual Perception

Abstract

Animals are constantly exposed to the time-varying visual world. Because visual perception is modulated by immediately prior visual experience, visual cortical neurons may register recent visual history into a specific form of offline activity and link it to later visual input. To examine how preceding visual inputs interact with upcoming information at the single neuron level, we designed a simple stimulation protocol in which a brief, orientated flashing stimulus was subsequently coupled to visual stimuli with identical or different features. Using in vivo whole-cell patch-clamp recording and functional two-photon calcium imaging from the primary visual cortex (V1) of awake mice, we discovered that a flash of sinusoidal grating per se induces an early, transient activation as well as a long-delayed reactivation in V1 neurons. This late response, which started hundreds of milliseconds after the flash and persisted for approximately 2 s, was also observed in human V1 electroencephalogram. When another drifting grating stimulus arrived during the late response, the V1 neurons exhibited a sublinear, but apparently increased response, especially to the same grating orientation. In behavioral tests of mice and humans, the flashing stimulation enhanced the detection power of the identically orientated visual stimulation only when the second stimulation was presented during the time window of the late response. Therefore, V1 late responses likely provide a neural basis for admixing temporally separated stimuli and extracting identical features in time-varying visual environments.

Cortical inactivation does not block response enhancement in the superior colliculus

“…Flashing stimuli compared to drifting sinusoidal gratings or reversal checkerboards are rather strong stimuli, thus can evoke changes faster. It was shown before that in adult mice flashing stimuli robustly evoke long-term changes in the V1 neuronal response and increase the broadband power of LFP signal [30,31]. Thus, the flash stimulus might be successfully used for the induction of modulation in the neuronal response [32], which we confirmed in our study.…”

Visual exposure enhances stimulus encoding and persistence in primary cortex

“…Previous studies have shown that brief stimulus presentations at high contrast produce strong persistent activity in primary visual cortex (Funayama et al, 2015;Huang et al, 2008). In our data, the flashed visual stimulus evoked a biphasic population response (example in Figure 1A), with an initial transient component which started immediately after stimulus onset and a delayed reverberatory component which started ~200 ms after stimulus offset.…”

“…Yet, stimulus-evoked responses in the primary visual cortex propagate through the local circuitry in wave-like patterns (Benucci et al, 2007;Xu et al, 2007, Grinvald Arieli and Janke) and can persist long after the cessation of stimulation (Benucci et al, 2009;Funayama et al, 2015;Huang et al, 2008;Nikolić et al, 2009). These complex and temporally-extended population responses have been implicated in reward timing (Chubykin et al, 2013;Gavornik et al, 2009;Shuler and Bear, 2006), working memory (Harrison and Tong, 2009;Munneke et al, 2010;Supèr et al, 2001) and are known to interact with (Benucci et al, 2009;Funayama et al, 2015;Gavornik and Bear, 2014;Nikolić et al, 2009;Wolff et al, 2017) and modulate the perception of (Brascamp et al, 2007;Fischer and Whitney, 2014;Funayama et al, 2015;Huang et al, 2008;Kahneman et al, 1992) subsequent visual stimulation. These dynamic properties exhibited by early visual neurons together with the exposure-dependent changes of stimulusresponses, suggest a direct involvement of primary visual cortex in the active distributed representation of more complex visual features, thus supporting a more constructive interpretation of primary cortex function (Olshausen and Field, 2005).…”

“…In particular, we examine how brief, repetitive exposure to a large set of abstract visual shapes (letters of the Latin alphabet and Arabic numerals), affects the capacity of a hypothetical downstream decoder to identify the presented stimulus based on population activity. We employ brief stimulus presentations at high contrast, known to induce strong reverberatory population activity (Funayama et al, 2015;Huang et al, 2008;Nikolić et al, 2009) and report exposure-driven changes in single-unit response properties, i.e. stimulus discrimination, firing rate magnitude and variability.…”

Multiple timescales account for adaptive responses across sensory cortices

“…5A). At lower frequencies (< 4 Hz), complex biphasic responses were common in S1 and V1, as has been previously reported in rodents and humans (Funayama et al, 2016;Funayama et al 2015;Sachidhanandam et al, 2013). We found, however that these multiphasic responses shifted to simple, monophasic responses as stimulus frequency increased to 4 Hz.…”