Enhanced behavioral performance through interareal gamma and beta synchronization.

Cognitive functioning requires coordination between brain areas. Between visual areas, feedforward gamma synchronization improves behavioral performance. Here, we investigate whether similar principles hold across brain regions and frequency bands, using simultaneous electrocorticographic recordings from 15 areas of two macaque monkeys during performance of a selective attention task. Short behavioral reaction times (RTs), suggesting efficient interareal communication, occurred when occipital areas V1, V2, V4, and DP showed gamma synchronization, and fronto-central areas S1, 5, F1, F2, and F4 showed beta synchronization. For both area clusters and corresponding frequency bands, deviations from the typically observed phase relations increased RTs. Across clusters and frequency bands, good phase relations occurred in a correlated manner specifically when they processed the behaviorally relevant stimulus. Furthermore, the fronto-central cluster exerted a beta-band influence onto the occipital cluster whose strength predicted short RTs. These results suggest that local gamma and beta synchronization and their inter-regional coordination jointly improve behavioral performance.

Enhanced Behavioral Performance through Interareal Gamma and Beta Synchronization.

Cognitive functioning requires coordination between brain areas. Between visual areas, feedforward gamma synchronization improves behavioral performance. Here, we investigate whether similar principles hold across brain regions and frequency bands, using simultaneous local field potential recordings from 15 areas during performance of a selective attention task. Short behavioral reaction times (RTs), an index of efficient interareal communication, occurred when occipital areas V1, V2, V4, DP showed gamma synchronization, and fronto-central areas S1, 5, F1, F2, F4 showed beta synchronization. For both area clusters and corresponding frequency bands, deviations from the typically observed phase relations increased RTs. Across clusters and frequency bands, good phase relations occurred in a correlated manner specifically when they processed the behaviorally relevant stimulus. Furthermore, the fronto-central cluster exerted a beta-band influence onto the occipital cluster whose strength predicted short RTs. These results suggest that local gamma and beta synchronization and their inter-regional coordination jointly improve behavioral performance.

Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise.

Circuits of excitatory and inhibitory neurons generate gamma-rhythmic activity (30-80 Hz). Gamma-cycles show spontaneous variability in amplitude and duration. To investigate the mechanisms underlying this variability, we recorded local-field-potentials (LFPs) and spikes from awake macaque V1. We developed a noise-robust method to detect gamma-cycle amplitudes and durations, which showed a weak but positive correlation. This correlation, and the joint amplitude-duration distribution, is well reproduced by a noise-driven damped harmonic oscillator. This model accurately fits LFP power-spectra, is equivalent to a linear, noise-driven E-I circuit, and recapitulates two additional features of gamma: (1) Amplitude-duration correlations decrease with oscillation strength; (2) amplitudes and durations exhibit strong and weak autocorrelations, respectively, depending on oscillation strength. Finally, longer gamma-cycles are associated with stronger spike-synchrony, but lower spike-rates in both (putative) excitatory and inhibitory neurons. In sum, V1 gamma-dynamics are well described by the simplest possible model of gamma: A damped harmonic oscillator driven by noise.

Brain rhythms define distinct interaction networks with differential dependence on anatomy.

Cognitive functions are subserved by rhythmic neuronal synchronization across widely distributed brain areas. In 105 area pairs, we investigated functional connectivity (FC) through coherence, power correlation, and Granger causality (GC) in the theta, beta, high-beta, and gamma rhythms. Between rhythms, spatial FC patterns were largely independent. Thus, the rhythms defined distinct interaction networks. Importantly, networks of coherence and GC were not explained by the spatial distributions of the strengths of the rhythms. Those networks, particularly the GC networks, contained clear modules, with typically one dominant rhythm per module. To understand how this distinctiveness and modularity arises on a common anatomical backbone, we correlated, across 91 area pairs, the metrics of functional interaction with those of anatomical projection strength. Anatomy was primarily related to coherence and GC, with the largest effect sizes for GC. The correlation differed markedly between rhythms, being less pronounced for the beta and strongest for the gamma rhythm.

Gamma Synchronization between V1 and V4 Improves Behavioral Performance.

Behavior is often driven by visual stimuli, relying on feedforward communication from lower to higher visual areas. Effective communication depends on enhanced interareal coherence, but it remains unclear whether this coherence occurs at an optimal phase relation that actually improves stimulus transmission to behavioral report. We recorded local field potentials from V1 and V4 of macaques performing an attention task during which they reported changes in the attended stimulus. V1-V4 gamma synchronization immediately preceding the stimulus change partly predicted subsequent reaction times (RTs). RTs slowed systematically as trial-by-trial interareal gamma phase relations deviated from the phase relation at which V1 and V4 synchronized on average. V1-V4 gamma phase relations accounted for RT differences of 13-31 ms. Effects were specific to the attended stimulus and not explained by local power or phase. Thus, interareal gamma synchronization occurs at the optimal phase relation for transmission of sensory inputs to motor responses.

A theta rhythm in macaque visual cortex and its attentional modulation.

Theta rhythms govern rodent sniffing and whisking, and human language processing. Human psychophysics suggests a role for theta also in visual attention. However, little is known about theta in visual areas and its attentional modulation. We used electrocorticography (ECoG) to record local field potentials (LFPs) simultaneously from areas V1, V2, V4, and TEO of two macaque monkeys performing a selective visual attention task. We found a ≈4-Hz theta rhythm within both the V1-V2 and the V4-TEO region, and theta synchronization between them, with a predominantly feedforward directed influence. ECoG coverage of large parts of these regions revealed a surprising spatial correspondence between theta and visually induced gamma. Furthermore, gamma power was modulated with theta phase. Selective attention to the respective visual stimulus strongly reduced these theta-rhythmic processes, leading to an unusually strong attention effect for V1. Microsaccades (MSs) were partly locked to theta. However, neuronal theta rhythms tended to be even more pronounced for epochs devoid of MSs. Thus, we find an MS-independent theta rhythm specific to visually driven parts of V1-V2, which rhythmically modulates local gamma and entrains V4-TEO, and which is strongly reduced by attention. We propose that the less theta-rhythmic and thereby more continuous processing of the attended stimulus serves the exploitation of this behaviorally most relevant information. The theta-rhythmic and thereby intermittent processing of the unattended stimulus likely reflects the ecologically important exploration of less relevant sources of information.

Visual areas exert feedforward and feedback influences through distinct frequency channels.

Visual cortical areas subserve cognitive functions by interacting in both feedforward and feedback directions. While feedforward influences convey sensory signals, feedback influences modulate feedforward signaling according to the current behavioral context. We investigated whether these interareal influences are subserved differentially by rhythmic synchronization. We correlated frequency-specific directed influences among 28 pairs of visual areas with anatomical metrics of the feedforward or feedback character of the respective interareal projections. This revealed that in the primate visual system, feedforward influences are carried by theta-band (∼ 4 Hz) and gamma-band (∼ 60-80 Hz) synchronization, and feedback influences by beta-band (∼ 14-18 Hz) synchronization. The functional directed influences constrain a functional hierarchy similar to the anatomical hierarchy, but exhibiting task-dependent dynamic changes in particular with regard to the hierarchical positions of frontal areas. Our results demonstrate that feedforward and feedback signaling use distinct frequency channels, suggesting that they subserve differential communication requirements.