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Abstract

A prominent feature of brain activity is oscillatory neuronal synchronization in the gamma range (40 – 90 Hz). Gamma rhythms have been hypothesized to implement the effective neuronal communication of selected stimuli through the alignment of excitability phases between lower and higher visual areas. Local gamma synchronization entails sequences of excitation and inhibition that have the potential to rhythmically modulate synaptic input gain. If synaptic inputs were consistently aligned to phases of high excitability, this would increase their gain. Indeed, we have previously shown that visually induced gamma in awake macaque area V4 and optogenetically induced gamma in anesthetized cat area 17 entails rhythmic gain modulation. Here, we tested whether visually induced gamma in awake macaque area V1 entails corresponding gain changes, and whether they constitute modulations of input or response gain.We recorded multi-unit activity (MUA) and local field potentials (LFP) from primary visual cortex (V1) of one awake macaque monkey. While the monkey maintained fixation, a uniform red background induced ongoing gamma-band activity, and a randomly timed probe stimulus evoked a MUA response. We investigated whether this MUA response was modulated by the phase of the ongoing gamma rhythm just prior to the probe presentation. Importantly, we quantified whether this putative gamma-rhythmic MUA-response modulation was multiplicative. That is, we tested, whether it exceeded an additive modulation that was expected from a simple superposition of an un-modulated probe-evoked response onto the background-induced ongoing gamma-rhythmic MUA modulation. Indeed, we found that gamma rhythmically modulated the MUA response, and that this modulation exceeded the additive component and therefore had a significant multiplicative component.We tested whether this effect constituted a gamma- rhythmic modulation of response gain or input gain. In the case of input gain, the contrast- response function is shifted to the left, with strongest response increases for mid-level stimulus contrasts. In the case of response gain, the contrast-response function is multiplied by an approximately constant factor for all stimulus contrasts. We therefore used probe stimuli with contrasts of 5%, 10%, 20%, 40%, 80% and 100%. The gamma-rhythmic gain modulation was approximately proportional to the probe-evoked response and thereby constituted a response- gain modulation.Based on these findings we propose that the gamma rhythm has causal consequences for neuronal communication, and that this effect is present in the primate visual system as early as primary visual cortex.