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      Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex

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      PLoS Biology
      Public Library of Science

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          High-gamma (80–200 Hz) activity can be dissociated from gamma rhythms in the monkey cortex, and appears largely to reflect spiking activity in the vicinity of the electrode.


          During cognitive tasks electrical activity in the brain shows changes in power in specific frequency ranges, such as the alpha (8–12 Hz) or gamma (30–80 Hz) bands, as well as in a broad range above ∼80 Hz, called the high-gamma band. The role or significance of this broadband high-gamma activity is unclear. One hypothesis states that high-gamma oscillations serve just like gamma oscillations, operating at a higher frequency and consequently at a faster timescale. Another hypothesis states that high-gamma power is related to spiking activity. Because gamma power and spiking activity tend to co-vary during most stimulus manipulations (such as contrast modulations) or cognitive tasks (such as attentional modulation), it is difficult to dissociate these two hypotheses. We studied the relationship between high-gamma power, gamma rhythm, and spiking activity in the primary visual cortex (V1) of awake monkeys while varying the stimulus size, which increased the gamma power but decreased the firing rate, permitting a dissociation. We found that gamma power became anti-correlated with the high-gamma power, suggesting that the two phenomena are distinct and have different origins. On the other hand, high-gamma power remained tightly correlated with spiking activity under a wide range of stimulus manipulations. We studied this relationship using a signal processing technique called Matching Pursuit and found that action potentials are associated with sharp transients in the LFP with broadband power, which is visible at frequencies as low as ∼50 Hz. These results distinguish broadband high-gamma activity from gamma rhythms as an easily obtained and reliable electrophysiological index of neuronal firing near the microelectrode. Further, they highlight the importance of making a careful dissociation between gamma rhythms and spike-related transients that could be incorrectly decomposed as rhythms using traditional signal processing methods.

          Author Summary

          Electrical activity in the brain often shows oscillations at distinct frequencies, such as the alpha (8–12 Hz) or gamma (30–80 Hz) bands, which have been linked with distinct cognitive states. In addition, changes in power are seen in a broad range above ∼80 Hz, called the “high-gamma” band. High-gamma power could arise either from sustained oscillations (similar to gamma rhythms but operating at higher frequencies) or from brief bursts of power associated with spikes generated near the electrode (“spike bleed-through”). It is difficult to dissociate these two hypotheses because gamma oscillations and spiking are correlated during most stimulus or cognitive manipulations. Further, most signal processing techniques decompose any signal into a set of oscillatory functions, making it difficult to represent any transient power fluctuations that occur at the time of spikes. We address the first issue by using a stimulus manipulation for which gamma oscillations and spiking activity are anti-correlated, permitting dissociation. To address the second issue, we use a signal processing technique called Matching Pursuit, which is well suited to capture transient activity. We show that gamma and high-gamma power become anti-correlated, suggesting different biophysical origins. Spikes and high-gamma power, however, remain tightly correlated. Broadband high-gamma activity could therefore be an easily obtained and reliable electrophysiological index of neuronal firing in the vicinity of an electrode.

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          Most cited references40

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          Spectrum estimation and harmonic analysis

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            Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks.

            Gamma frequency oscillations are thought to provide a temporal structure for information processing in the brain. They contribute to cognitive functions, such as memory formation and sensory processing, and are disturbed in some psychiatric disorders. Fast-spiking, parvalbumin-expressing, soma-inhibiting interneurons have a key role in the generation of these oscillations. Experimental analysis in the hippocampus and the neocortex reveals that synapses among these interneurons are highly specialized. Computational analysis further suggests that synaptic specialization turns interneuron networks into robust gamma frequency oscillators.
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              Attention improves performance primarily by reducing interneuronal correlations

              Visual attention can dramatically improve behavioural performance by allowing observers to focus on the important information in a complex scene. Attention also typically increases the firing rates of cortical sensory neurons. Rate increases improve the signal-to-noise ratio of individual neurons, and this improvement has been assumed to underlie attention-related improvements in behaviour. We recorded dozens of neurons simultaneously in visual area V4 and found that changes in single neurons accounted for only a small fraction of the improvement in the sensitivity of the population. Instead, over 80% of the attentional improvement in the population signal was caused by decreases in the correlations between the trial-to-trial fluctuations in the responses of pairs of neurons. These results suggest that the representation of sensory information in populations of neurons and the way attention affects the sensitivity of the population may only be understood by considering the interactions between neurons.

                Author and article information

                Role: Academic Editor
                PLoS Biol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                April 2011
                April 2011
                12 April 2011
                : 9
                : 4
                [1]Department of Neurobiology & Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts, United States of America
                National Institutes of Mental Health, United States of America
                Author notes

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: SR JHRM. Performed the experiments: SR. Analyzed the data: SR. Wrote the paper: SR JHRM.

                Ray, Maunsell. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 15
                Research Article
                Neuroscience/Sensory Systems

                Life sciences
                Life sciences


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