Opinion
Do gamma oscillations play a role in cerebral cortex?

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Highlights

  • Cortical gamma rhythms have low and inconsistent power.

  • Cortical gamma rhythms are affected by low-level stimulus features.

  • Coordinating gamma phase across multiple areas is difficult given conduction delays.

  • Spike-related activity can bias phase estimation between gamma and spiking.

Gamma rhythm (which has a center frequency between 30 and 80 Hz) is modulated by cognitive mechanisms such as attention and memory, and has been hypothesized to play a role in mediating these processes by supporting communication channels between cortical areas or encoding information in its phase. We highlight several issues related to gamma rhythms, such as low and inconsistent power, its dependence on low-level stimulus features, problems due to conduction delays, and contamination due to spike-related activity that makes accurate estimation of gamma phase difficult. Gamma rhythm could be a potentially useful signature of excitation–inhibition interactions in the brain, but whether it also provides a mechanism for information processing or coding remains an open question.

Section snippets

Gamma rhythms in the brain

Electrical signals recorded from the brain often show oscillations spanning a broad range of frequencies, which are highly conserved across species and are associated with distinct cognitive states 1, 2. Gamma rhythm, which is an oscillation concentrated in a range of ∼20 Hz with a center frequency between 30 and 80 Hz, has been consistently linked with high-level cognitive functions such attention 3, 4, 5, 6, memory 7, 8, 9, and perception 10, 11, which has led to proposals that gamma plays a

Generation, functional roles, and alternative hypotheses

It is well established that inhibition, especially through parvalbumin-positive fast spiking basket cells, plays a crucial role in the generation of gamma rhythms 16, 17, 18, 19, 20, 21. A network of inhibitory interneurons that fires rhythmically can induce periodic fluctuations in the intracellular potential of pyramidal cells, such that the excitability of those cells varies within each cycle of the rhythm. The inhibitory network could generate the rhythm by itself or through periodic

Low and inconsistent power

Proposals such as CTC and PC are easy to implement when the signal energy at the frequency of interest is much higher than other frequencies 50, 51, which can be the case for low-frequency rhythms such as alpha or theta (Box 1). However, all biological rhythms have a 1/f power form, such that the signal power typically falls off with the inverse of the frequency. Figure 2A shows the time frequency power spectrum under very favorable conditions for producing gamma oscillations. Figure 2B shows

Conduction delays

Another difficulty with exploiting gamma rhythms for information processing is the relatively slow propagation of neuronal signals in cortex. Although fast-conducting axons can transmit spikes at tens of meters per second, there are substantial delays in the relay of signals within and between cortical areas (see e.g., Figure 2 and Table 1 in [71] for a detailed comparison of stimulus onset latency across several visual areas). In monkey visual cortex, the earliest responses of visual neurons

Stimulus dependence of gamma

For gamma to play a functional role in communication or PC, it is desirable that the amplitude or frequency of gamma should not depend on the properties of the stimulus itself. However, gamma depends greatly and systematically on a variety of stimulus features [25] (Figure 3A–D) including size 56, 76, 77, contrast 31, 78, 79, noise [80], orientation 56, 81, 82, spatial frequency [83], speed 84, 85, 86, direction [87], and eccentricity 88, 89. It also depends on the properties of the brain, such

Spike-related transients affect gamma phase estimation

In CTC or PC, gamma rhythms adjust the coordination or timing of a spike, and testing this hypothesis therefore entails a proper estimation of gamma phase with respect to the spike. This is a methodological problem that the experimenter faces. Further, these hypotheses assume that the spike itself does not change the properties of the gamma channel because this would cause the properties of the carrier to be modified depending on the content. However separating the carrier and content is

Concluding remarks

In summary, we raise several signal-processing issues regarding gamma oscillations. First, they have low power, typically less than 10% of the total signal power, are absent during baseline, and are too weak to serve any role during the first ∼200 ms after stimulus onset. Special filtering techniques are needed to use these signals for coding, for which there is little evidence. Second, long conduction delays pose serious issues in matching gamma phase across distributed brain areas. Third,

Acknowledgments

We thank Drs Adam Kohn and Gyorgy Buzsáki for their insightful comments. This work was supported by the Wellcome Trust/DBT India Alliance (Intermediate Fellowship to S.R.) and National Institutes of Health (NIH) grant R01EY005911 (to J.H.R.M.).

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