Robust gamma coherence between macaque V1 and V2 by dynamic frequency matching

Roberts, M. J., Lowet, E., Brunet, N. M., Ter Wal, M., Tiesinga, P., Fries, P., & De Weerd, P. (2013)

Neuron, 78(3), 523-536.


Current theories propose that coherence of oscillatory brain activity in the gamma band (30-80 Hz) constitutes an avenue for communication among remote neural populations. However, reports documenting stimulus dependency and time variability of gamma frequency suggest that distant neuronal populations may, at any one time, operate at different frequencies precluding synchronization. To test this idea, we recorded from macaque V1 and V2 simultaneously while presenting gratings of varying contrast. Although gamma frequency increased with stimulus contrast in V1 and V2 (by ∼25 Hz), V1-V2 gamma coherence was maintained for all contrasts. Moreover, while gamma frequency fluctuated by ∼15 Hz during constant contrast stimulation, this fluctuation was highly correlated between V1 and V2. The strongest coherence connections showed a layer-specific pattern, matching feedforward anatomical connectivity. Hence, gamma coherence among remote populations can occur despite large stimulus-induced and time-dependent changes in gamma frequency, allowing communication through coherence to operate without a stimulus independent, fixed-frequency gamma channel.

Contribution to the field

Influential theories of synchronization (such as Communication through Coherence, or CTC, by P. Fries) propose that neural communication is based on phase locking at an appropriate phase difference, while assuming that oscillation frequency is constant. In this context, the present paper has two main contributions. First (in line with other research) it showed a large effect of contrast on gamma frequency, and additionally large moment-to-moment fluctuations in gamma frequency. These findings had been used by others to suggest that gamma could no longer be considered a vehicle for communication in the brain.  In contrast with that idea, the second relevant finding was that despite these stimulus-related and random variations in frequency, there was strong coherence between V1 and V2, which moreover occurred in a layer-specific manner consistent with feedforward information processing (as also confirmed with a Granger Causality measure of directionality). In line with this, we found gamma frequency fluctuations between V1 and V2 to be highly correlated. These findings gave us the first intuition that there had to be active frequency matching mechanisms enabling consistent phase relations underlying synchronization despite these frequency fluctuations.

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