A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior

Bosman, Conrado A.; Womelsdorf, Thilo; Desimone, Robert; Fries, Pascal

doi:10.1523/jneurosci.1193-09.2009

Cited by 214 publications

(312 citation statements)

References 68 publications

(137 reference statements)

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“…This result is in line with a recent animal study that provided eye movement control at a much higher resolution using scleral search coil techniques (Ignashchenkova et al, 2009). Improvements in experimental control notwithstanding, two features of fixation have not been addressed so far by the studies on motion perception in cerebellar patients, i.e., the occurrence of microsaccades, recently suggested to play a role in visual perception (Bosman et al, 2009), and fixation alignment between the two eyes, a faculty that can indeed be compromised after cerebellar lesioning (Versino et al, 1996;Straube et al, 2009).…”

Section: Discussionsupporting

confidence: 82%

Visual Motion Perception Deficits Due to Cerebellar Lesions Are Paralleled by Specific Changes in Cerebro-Cortical Activity

Händel¹,

Thier²,

Haarmeier³

2009

J. Neurosci.

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Recent anatomical studies have revealed strong cerebellar projections into parietal and prefrontal cortex. These findings suggest that the cerebellum might not only play a functional role in motor control but also cognitive domains, an idea also supported by neuropsychological testing of patients with cerebellar lesions that has revealed specific deficits. The goal of the present study was to test whether or not cognitive impairments after cerebellar damage are resulting from changes in cerebro-cortical signal processing. The detection of global visual motion embedded in noise, a faculty compromised after cerebellar lesions, was chosen as a model system. Using magnetoencephalography, cortical responses were recorded in a group of patients with cerebellar lesions (n ϭ 8) and controls (n ϭ 13) who observed visual motion of varied coherence, i.e., motion strength, presented in the peripheral visual field during controlled stationary fixation. Corroborating earlier results, the patients showed a significant impairment in global motion discrimination despite normal fixation behavior. This deficit was paralleled by qualitative differences in responses recorded from parieto-temporal cortex, including a reduced responsiveness to coherent visual motion and a striking loss of bilateral representations of motion coherence. Moreover, the perceptual thresholds correlated with the cortical representation of motion strength on single subject basis. These results demonstrate that visual motion processing in cerebral cortex critically depends on an intact cerebellum and establish a correlation between cortical activity and impaired visual perception resulting from cerebellar damage.

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Section: Discussionsupporting

confidence: 82%

Visual Motion Perception Deficits Due to Cerebellar Lesions Are Paralleled by Specific Changes in Cerebro-Cortical Activity

Händel¹,

Thier²,

Haarmeier³

2009

J. Neurosci.

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“…Finally, we note that high-frequency synchronization is often modulated by the phase of low-frequency rhythms (Bragin et al, 1995;Lakatos et al, 2005;Canolty et al, 2006;Bosman et al, 2009;Fries, 2009a;Schroeder and Lakatos, 2009). Low-frequency rhythms even appear to switch between alternative spatial gamma-synchronization patterns (Colgin et al, 2009;Fries, 2009b).…”

Section: Discussionmentioning

confidence: 81%

Corticospinal Beta-Band Synchronization Entails Rhythmic Gain Modulation

Elswijk¹,

Maij²,

Schoffelen³

et al. 2010

J. Neurosci.

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102

100

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Rhythmic synchronization of neurons in the beta or gamma band occurs almost ubiquitously, and this synchronization has been linked to numerous nervous system functions. Many respective studies make the implicit assumption that neuronal synchronization affects neuronal interactions. Indeed, when neurons synchronize, their output spikes reach postsynaptic neurons together, trigger coincidence detection mechanisms, and therefore have an enhanced impact. There is ample experimental evidence demonstrating this consequence of neuronal synchronization, but beyond this, beta/gamma-band synchronization within a group of neurons might also modulate the impact of synaptic input to that synchronized group. This would constitute a separate mechanism through which synchronization affects neuronal interactions, but direct in vivo evidence for this putative mechanism is lacking. Here, we demonstrate that synchronized beta-band activity of a neuronal group modulates the efficacy of synaptic input to that group in-phase with the beta rhythm. This response modulation was not an addition of rhythmic activity onto the average response but a rhythmic modulation of multiplicative input gain. Our results demonstrate that beta-rhythmic activity of a neuronal target group multiplexes input gain along the rhythm cycle. The actual gain of an input then depends on the precision and the phase of its rhythmic synchronization to this target, providing one mechanistic explanation for why synchronization modulates interactions.

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“…Regarding the theta band, we note that the visual cortical theta rhythm is partly locked to microsaccades 22 . Therefore, theta-rhythmic microsaccades with corresponding retinal image motion and subsequent visual responses might contribute to the feedforward GC influences in the theta band.…”

Section: Cc-by-nc-nd 40 International License Not Peer-reviewed) Is mentioning

confidence: 89%

Visual areas exert feedforward and feedback influences through distinct frequency channels

Bastos

Vezoli

Bosman

et al. 2014

Preprint

178

284

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However, although these studies have revealed the anatomical paths and the neurophysiological consequences of influences in both directions, the neurophysiological mechanisms through which these influences are exerted remain largely elusive. Here we show that in the primate visual system, feedforward influences are carried by thetaband (~4 Hz) and gamma-band (~60-80 Hz) synchronization, and feedback influences by beta-band (~14-18 Hz) synchronization. These frequency-specific asymmetries in directed influences were revealed by simultaneous local field potential recordings from eight visual areas and an analysis of Granger-causal influences across all 28 pairs of areas. The asymmetries in directed influences correlated directly with asymmetries in anatomy and enabled us to build a visual cortical hierarchy from the influence asymmetries alone. Across different task periods, most areas stayed at their hierarchical position, whereas particularly frontal areas moved dynamically. Our results demonstrate that feedforward and feedback signalling use different frequency channels, which might subserve their differential communication requirements and lead to differential local consequences. The possibility to infer hierarchical relationships through functional data alone might make it possible to derive a cortical hierarchy in the living human brain.Many aspects of cognitive performance can only be explained through the concept of feedback influences. For example, reaction times are shortened when stimulus locations are pre-cued and attention can be pre-directed, an effect that cannot be explained if only constant feedforward input is considered 3 . Numerous neurophysiological studies have demonstrated the effects of feedback influences on neuronal activity 2 , yet the mechanisms through which feedback influences are exerted remain elusive. Anatomical studies have revealed that structural connections in the feedforward direction, i.e. from the primary sensory areas to higher order areas, are complemented by connections in the feedback direction 1,4 . In addition, it is well established that feedforward and feedback connections follow a characteristic pattern with regard to cortical layers: Feedforward connections target the granular layer 1 ; they originate preferentially in supragranular layers, and this preference is stronger for projections traversing more hierarchical levels, i.e. it is quantitatively related to the hierarchical distance 4 .Feedback connections avoid targeting the granular layer 1 ; they originate preferentially in the infragranular layers, and again, this preference is stronger for projections traversing more hierarchical levels and is thereby quantitatively related to hierarchical distance 4 . These asymmetries have been used to arrange the visual cortical areas into a hierarchy 1,4 , which has influenced many theories of cognition and brain function 5,6 .Recent studies have documented a neurophysiological asymmetry between cortical layers in visual cortex: While supragranular layers show local gam...

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A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior

Cited by 214 publications

References 68 publications

Visual Motion Perception Deficits Due to Cerebellar Lesions Are Paralleled by Specific Changes in Cerebro-Cortical Activity

Visual Motion Perception Deficits Due to Cerebellar Lesions Are Paralleled by Specific Changes in Cerebro-Cortical Activity

Corticospinal Beta-Band Synchronization Entails Rhythmic Gain Modulation

Visual areas exert feedforward and feedback influences through distinct frequency channels

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