Shifts of Gamma Phase across Primary Visual Cortical Sites Reflect Dynamic Stimulus-Modulated Information Transfer

Abstract

Distributed neural processing likely entails the capability of networks to reconfigure dynamically the directionality and strength of their functional connections. Yet, the neural mechanisms that may allow such dynamic routing of the information flow are not yet fully understood. We investigated the role of gamma band (50–80 Hz) oscillations in transient modulations of communication among neural populations by using measures of direction-specific causal information transfer. We found that the local phase of gamma-band rhythmic activity exerted a stimulus-modulated and spatially-asymmetric directed effect on the firing rate of spatially separated populations within the primary visual cortex. The relationships between gamma phases at different sites (phase shifts) could be described as a stimulus-modulated gamma-band wave propagating along the spatial directions with the largest information transfer. We observed transient stimulus-related changes in the spatial configuration of phases (compatible with changes in direction of gamma wave propagation) accompanied by a relative increase of the amount of information flowing along the instantaneous direction of the gamma wave. These effects were specific to the gamma-band and suggest that the time-varying relationships between gamma phases at different locations mark, and possibly causally mediate, the dynamic reconfiguration of functional connections.

Cortical travelling waves: mechanisms and computational principles

“…While initial evidence indicated that travelling waves were pronounced only in weak input regimes 21,22 , recent studies have shown that travelling waves are evoked following small, high-contrast visual stimuli 14 , and they appear to play a role in cortical dynamics driven by dynamic sensory input and sensorimotor planning 30 . It has previously been noted that the existence of stimulus-evoked travelling waves in the sensory cortex presents a challenge to the orderly topographic arrangement of selectivity first described by Hubel and Wiesel at the trial-averaged level 22 .…”

“…This suggests that these multicycle high-frequency oscillations ride on top of a broader stimulus-evoked travelling wave and form sustained complex patterns that reflect features of the input. Furthermore, using a measure of directed information transfer across recording sites, a recent study found that shifts of the phase of gamma oscillations between pairs of electrodes in V1 of anaesthetized primates during stimulation with Hollywood movies are consistent with the presence of complex travelling waves propagating in the direction of maximal information transfer 30 . Importantly, these interactions were consistent with propagation along the horizontal-fibre network and not with input changes, illustrating that the effect of the horizontal-fibre networks in the visual cortex (and their intrinsic time delays) does not disappear in more naturalistic high-input situations.…”

“…Analysis of multichannel recordings will make it possible to test whether stimulus position and timing can be reliably decoded from responses at the single-trial level. While it has been noted that cortical travelling waves may structure visual responses to dynamic natural scenes 30 , it remains unclear how the spatiotemporal interactions revealed following simple sensory stimuli 14 generalize to multi-stimulus paradigms and natural scenes. Nevertheless, the effect of the abundant horizontal connections highlighted in this work (and their intrinsic axonal time delays) is not expected to disappear.…”

“…They travel over spatial scales that range from the mesoscopic (single cortical areas and millimetres of cortex) to the macroscopic (global patterns of activity over several centimetres) and extend over temporal scales from tens to hundreds of milliseconds. Although, in initial studies, mesoscopic travelling waves were pronounced only under conditions of low visual luminance contrast 21,22 and were mostly reported in anaesthetized states 23–28 , recent work has shown that stimulus-evoked mesoscopic travelling waves robustly appear in the awake visual cortex 14,29 and can influence intracortical dynamics during the viewing of natural stimuli 30 .…”

Coherent alpha oscillations link current and future receptive fields during saccades

“…Less is known about flexible communication within individual brain regions, but there is reason to suspect that it is useful as well (7)(8)(9). For instance, in sensory systems, space is represented in the form of maps that encode the location of individual stimuli.…”