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Functional neurosurgery has afforded the opportunity to assess interactions between populations of neurons in the human cerebral cortex and basal ganglia in patients with Parkinson's disease (PD). Interactions occur over a wide range of frequencies, and the functional significance of those >30 Hz is particularly unclear. Do they improve movement, and, if so, in what way? We acquired simultaneously magnetoencephalography and direct recordings from the subthalamic nucleus (STN) in 17 PD patients. We examined the effect of synchronous and sequential finger movements and of the dopamine prodrug levodopa on induced power in the contralateral primary motor cortex (M1) and STN and on the coherence between the two structures. We observed discrete peaks in M1 and STN power at 60-90 Hz and at 300-400 Hz. All these power peaks increased with movement and levodopa treatment. Only STN activity at 60-90 Hz was coherent with activity in M1. Directionality analysis showed that STN gamma activity at 60-90 Hz tended to drive gamma activity in M1. The effects of levodopa on both local and distant synchronization at 60-90 Hz correlated with the degree of improvement in bradykinesia-rigidity as did local STN activity at 300-400 Hz. Despite this, there were no effects of movement type, nor interactions between movement type and levodopa in the STN, nor in the coherence between STN and M1. We conclude that synchronization at 60-90 Hz in the basal ganglia cortical network is prokinetic but likely through a modulatory effect rather than any involvement in explicit motor processing.

Local groups of neurons engaged in a cognitive task often exhibit rhythmically synchronized activity in the gamma band, a phenomenon that likely enhances their impact on downstream areas. The efficacy of neuronal interactions may be enhanced further by interareal synchronization of these local rhythms, establishing mutually well timed fluctuations in neuronal excitability. This notion suggests that long-range synchronization is enhanced selectively for connections that are behaviorally relevant. We tested this prediction in the human motor system, assessing activity from bilateral motor cortices with magnetoencephalography and corresponding spinal activity through electromyography of bilateral hand muscles. A bimanual isometric wrist extension task engaged the two motor cortices simultaneously into interactions and coherence with their respective corresponding contralateral hand muscles. One of the hands was cued before each trial as the response hand and had to be extended further to report an unpredictable visual go cue. We found that, during the isometric hold phase, corticomuscular coherence was enhanced, spatially selective for the corticospinal connection that was effectuating the subsequent motor response. This effect was spectrally selective in the low gamma-frequency band (40-47 Hz) and was observed in the absence of changes in motor output or changes in local cortical gamma-band synchronization. These findings indicate that, in the anatomical connections between the cortex and the spinal cord, gamma-band synchronization is a mechanism that may facilitate behaviorally relevant interactions between these distant neuronal groups.

Work on animals indicates that BOLD is preferentially sensitive to local field potentials, and that it correlates most strongly with gamma band neuronal synchronization. Here we investigate how the BOLD signal in humans performing a cognitive task is related to neuronal synchronization across different frequency bands. We simultaneously recorded EEG and BOLD while subjects engaged in a visual attention task known to induce sustained changes in neuronal synchronization across a wide range of frequencies. Trial-by-trial BOLD fluctuations correlated positively with trial-by-trial fluctuations in high-EEG gamma power (60-80 Hz) and negatively with alpha and beta power. Gamma power on the one hand, and alpha and beta power on the other hand, independently contributed to explaining BOLD variance. These results indicate that the BOLD-gamma coupling observed in animals can be extrapolated to humans performing a task and that neuronal dynamics underlying high- and low-frequency synchronization contribute independently to the BOLD signal., (Copyright © 2011 Elsevier Inc. All rights reserved.)

A single brief visual stimulus accompanied by two brief tactile stimuli is frequently perceived incorrectly as two flashes, a phenomenon called double-flash illusion (DFI). We investigated whether the DFI is accompanied by changes in rhythmic neuronal activity, using magnetoencephalography in human subjects. Twenty-two subjects received visuo-tactile stimulation and reported the number of perceived visual stimuli. We sorted trials with identical physical stimulation according to the reported subjective percept and assessed differences in spectral power in somatosensory and occipital sensors. In DFI trials, occipital sensors displayed a contralateral enhancement of gamma-band (80-140 Hz) activity in response to stimulation. In somatosensory sensors, the DFI was associated with an increase of spectral power for low frequencies (5-17.5 Hz) around stimulation and a decrease of spectral power in the 22.5-30 Hz range between 450 and 750 ms post-stimulation. In summary, several components of rhythmic activity predicted variable subjective experience for constant physical stimulation. Notably, the enhanced occipital gamma-band activity during DFI was similar in time and frequency extent to the somatosensory gamma-band response to tactile stimulation. We speculate that the DFI might therefore occur when the somatosensory gamma-response is transmitted to visual cortex. This transmission might be supported by the observed modulations in low-frequency activity., (Copyright © 2010 Elsevier Inc. All rights reserved.)

Gamma-band synchronization is abundant in nervous systems. Typically, the strength or precision of gamma-band synchronization is studied. However, the precise phase with which individual neurons are synchronized to the gamma-band rhythm might have interesting consequences for their impact on further processing and for spike timing-dependent plasticity. Therefore, we investigated whether the spike times of individual neurons shift systematically in the gamma cycle as a function of the neuronal activation strength. We found that stronger neuronal activation leads to spikes earlier in the gamma cycle, i.e., we observed gamma-phase shifting. Gamma-phase shifting occurred on very rapid timescales. It was particularly pronounced for periods in which gamma-band synchronization was relatively weak and for neurons that were only weakly coupled to the gamma rhythm. We suggest that gamma-phase shifting is brought about by an interplay between overall excitation and gamma-rhythmic synaptic input and has interesting consequences for neuronal coding, competition, and plasticity.

Oscillatory neuronal synchronization, within and between cortical areas, may mediate the selection of attended visual stimuli. However, it remains unclear at and between which processing stages visuospatial attention modulates oscillatory synchronization in the human brain. We thus combined magnetoencephalography (MEG) in a spatially cued motion discrimination task with source-reconstruction techniques and characterized attentional effects on neuronal synchronization across key stages of the human dorsal visual pathway. We found that visuospatial attention modulated oscillatory synchronization between visual, parietal, and prefrontal cortex in a spatially selective fashion. Furthermore, synchronized activity within these stages was selectively modulated by attention, but with markedly distinct spectral signatures and stimulus dependence between regions. Our data indicate that regionally specific oscillatory synchronization at most stages of the human dorsal visual pathway may enhance the processing of attended visual stimuli and suggest that attentional selection is mediated by frequency-specific synchronization between prefrontal, parietal, and early visual cortex.

Selective attention lends relevant sensory input priority access to higher-level brain areas and ultimately to behavior. Recent studies have suggested that those neurons in visual areas that are activated by an attended stimulus engage in enhanced gamma-band (30-70 Hz) synchronization compared with neurons activated by a distracter. Such precise synchronization could enhance the postsynaptic impact of cells carrying behaviorally relevant information. Previous studies have used the local field potential (LFP) power spectrum or spike-LFP coherence (SFC) to indirectly estimate spike synchronization. Here, we directly demonstrate zero-phase gamma-band coherence among spike trains of V4 neurons. This synchronization was particularly evident during visual stimulation and enhanced by selective attention, thus confirming the pattern inferred from LFP power and SFC. We therefore investigated the time course of LFP gamma-band power and found rapid dynamics consistent with interactions of top-down spatial and feature attention with bottom-up saliency. In addition to the modulation of synchronization during visual stimulation, selective attention significantly changed the prestimulus pattern of synchronization. Attention inside the receptive field of the recorded neuronal population enhanced gamma-band synchronization and strongly reduced alpha-band (9-11 Hz) synchronization in the prestimulus period. These results lend further support for a functional role of rhythmic neuronal synchronization in attentional stimulus selection.

Brain processing depends on the interactions between neuronal groups. Those interactions are governed by the pattern of anatomical connections and by yet unknown mechanisms that modulate the effective strength of a given connection. We found that the mutual influence among neuronal groups depends on the phase relation between rhythmic activities within the groups. Phase relations supporting interactions between the groups preceded those interactions by a few milliseconds, consistent with a mechanistic role. These effects were specific in time, frequency, and space, and we therefore propose that the pattern of synchronization flexibly determines the pattern of neuronal interactions.

Paired associative stimulation (PAS), which combines repetitive peripheral nerve stimulation with transcranial magnetic stimulation (TMS), may induce neuroplastic changes in somatosensory cortex (S1), possibly by long-term potentiation-like mechanisms. We used multichannel median nerve somatosensory evoked potential (MN-SSEP) recordings and two-point tactile discrimination testing to examine the location and behavioural significance of these changes. When TMS was applied to S1 near-synchronously to an afferent signal containing mechanoreceptive information, MN-SSEP changes (significant at 21–31 ms) could be explained by a change in a tangential source located in Brodmann area 3b, with their timing and polarity suggesting modification of upper cortical layers. PAS-induced MN-SSEP changes between 28 and 32 ms were linearly correlated with changes in tactile discrimination. Conversely, when the near-synchronous afferent signal contained predominantly proprioceptive information, PAS-induced MN-SSEP changes (20–29 ms) were shifted medially, and tactile performance remained stable. With near-synchronous mechanoreceptive stimulation subtle differences in the timing of the two interacting signals tended to influence the direction of tactile performance changes. PAS performed with TMS delivered asynchronously to the afferent pulse did not change MN-SSEPs. Hebbian interaction of mechanoreceptive afferent signals with TMS-evoked activity may modify synaptic efficacy in superficial cortical layers of Brodmann area 3b and is associated with timing-dependent and qualitatively congruent behavioural changes. [ABSTRACT FROM AUTHOR]

We investigated the effects of spatial-selective attention on oscillatory neuronal dynamics in a tactile delayed-match-to-sample task. Whole-head magnetoencephalography was recorded in healthy subjects while dot patterns were presented to their index fingers using Braille stimulators. The subjects' task was to report the reoccurrence of an initially presented sample pattern in a series of up to eight test stimuli that were presented unpredictably to their right or left index finger. Attention was cued to one side (finger) at the beginning of each trial, and subjects performed the task at the attended side, ignoring the unattended side. After stimulation, high-frequency gamma-band activity (60-95 Hz) in presumed primary somatosensory cortex (S1) was enhanced, whereas alpha- and beta-band activity were suppressed in somatosensory and occipital areas and then rebounded. Interestingly, despite the absence of any visual stimulation, we also found time-locked activation of medial occipital, presumably visual, cortex. Most relevant, spatial tactile attention enhanced stimulus-induced gamma-band activity in brain regions consistent with contralateral S1 and deepened and prolonged the stimulus induced suppression of beta- and alpha-band activity, maximal in parieto-occipital cortex. Additionally, the beta rebound over contralateral sensorimotor areas was suppressed. We hypothesize that spatial-selective attention enhances the saliency of sensory representations by synchronizing neuronal responses in early somatosensory cortex and thereby enhancing their impact on downstream areas and facilitating interareal processing. Furthermore, processing of tactile patterns also seems to recruit visual cortex and this even more so for attended compared with unattended stimuli. [ABSTRACT FROM AUTHOR]

Neuronal gamma-band synchronization is central for cognition. Respective studies in human subjects focused on a visually induced transient enhancement of broadband EEG power. In this issue of Neuron, Yuval-Greenberg et al. demonstrate that this EEG response is an artifact of microsaccades, raising the question of whether gamma-band synchronization can be assessed with EEG. [Copyright &y& Elsevier]

Summary 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. [ABSTRACT FROM AUTHOR]