Gamma-Rhythmic Gain Modulation

Abstract

Summary Cognition requires the dynamic modulation of effective connectivity, i.e. the modulation of the postsynaptic neuronal response to a given input. If postsynaptic neurons are rhythmically active, this might entail rhythmic gain modulation, such that inputs synchronized to phases of high gain benefit from enhanced effective connectivity. We show that visually induced gamma-band activity in awake macaque area V4 rhythmically modulates responses to unpredictable stimulus events. This modulation exceeded a simple additive superposition of a constant response onto ongoing gamma-rhythmic firing, demonstrating the modulation of multiplicative gain. Gamma phases leading to strongest neuronal responses also led to shortest behavioral reaction times, suggesting functional relevance of the effect. Furthermore, we find that constant optogenetic stimulation of anesthetized cat area 21a produces gamma-band activity entailing a similar gain modulation. As the gamma rhythm in area 21a did not spread backwards to area 17, this suggests that postsynaptic gamma is sufficient for gain modulation.

Signal transfer of visual stimuli to V4 occurs in gamma-rhythmic, pulsed information packages

“…As a direct implication, RBS posits that stimulus information arrives at V4 from lower visual areas in the form of periodically pulsed information packages, where the phase relationship between the rhythmic activities of the sending and receiving populations determines whether the packages get passed on or will be suppressed. Behavioral correlates compatible with such a pulsed information transfer were reported by two recent studies demonstrating that reaction times to a sudden stimulus change depend on both, the V4 gamma phase just before the transient response evoked in V4 by the stimulus change (Ni et al, 2016), and on the V1-V4 phase relationship preceding the stimulus change (Rohenkohl et al, 2018). These results are line with the assumption that transient input arriving during V4 excitability peaks could improve behavioral responses.…”

“…Synchronization in the activity of a presynaptic (sending) population increases its post-synaptic influence by making the neurons' spiking outputs coincident in time, an effect found to be enhanced for populations processing attended versus non-attended stimuli (Azouz and Gray, 2003;Bichot et al, 2005;Fries et al, 2001;Steinmetz et al, 2000;Taylor et al, 2005). For the post-synaptic receiver population, local oscillatory synchronization establishes a rhythmic modulation of gain, with alternating periods of high and low excitability (Atallah and Scanziani, 2009;Buzsáki and Wang, 2012;Ni et al, 2016;Salkoff et al, 2015;Vinck et al, 2013). Noteworthy, the amplitude of gamma oscillations is not constant, for instance showing modulation by a low-frequency rhythm in the 6-10 Hz range (Bosman et al, 2009;Fries, 2015;McLelland and VanRullen, 2016;Palmigiano et al, 2017;Spyropoulos et al, 2018).…”

Local entrainment of oscillatory activity induced by direct brain stimulation in humans

“…Second, we could also entertain the hypothesis that at difference with noninvasive stimulation methods2243 the highly focal and the very intense stimulation source provided by intracranial electrical stimulation has the potential to impose fast rhythms outside the boundaries of the “natural” frequency characterizing a given site. In support of the latter possibility, evidence from animal studies using frequency-tuned optogenetic stimulation6162, also support entrainment of neural oscillations regardless of the “natural” frequency operating in the stimulated region. The discussion of this point opens a fair debate on whether or not entrainment in a given area would be particularly facilitated when stimulation is tuned to the most “natural” frequency operating on the stimulated site.…”

A Principle for Describing and Verifying Brain Mechanisms Using Ongoing Activity

“…This increased coherence may in turn govern the communication through coherence theory in order to sustain the communication over time (Fries, 2005, 2015). Indeed, action potentials are gated if they arrive on a certain phase of an artificial oscillation in the target structure (Cardin et al, 2009; Siegle et al, 2014; Ni et al, 2016). Although this background input is crucial for describing the dynamic gating it has so far been overlooked (Figure 2C).…”