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The Journal of Neuroscience, July 29, 2009, 29(30):9471-9480; doi:10.1523/JNEUROSCI.1193-09.2009

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Behavioral/Systems/Cognitive
A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior

Conrado A. Bosman,1 Thilo Womelsdorf,1 Robert Desimone,2,3 and Pascal Fries1

1Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, 2Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, and 3McGovern Institute for Brain Research at the Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Correspondence should be addressed to Dr. Conrado Bosman, Donders Institute for Brain, Cognition and Behaviour, Centre of Cognitive Neuroimaging, Radboud University Nijmegen, Kapittelweg 29, 6525 EN Nijmegen, The Netherlands. Email: c.bosman{at}donders.ru.nl

Rhythms occur both in neuronal activity and in behavior. Behavioral rhythms abound at frequencies at or below 10 Hz. Neuronal rhythms cover a very wide frequency range, and the phase of neuronal low-frequency rhythms often rhythmically modulates the strength of higher-frequency rhythms, particularly of gamma-band synchronization (GBS). Here, we study stimulus-induced GBS in awake monkey areas V1 and V4 in relation to a specific form of spontaneous behavior, namely microsaccades (MSs), small fixational eye movements. We found that MSs occur rhythmically at a frequency of ~3.3 Hz. The rhythmic MSs were predicted by the phase of the 3.3 Hz rhythm in V1 and V4 local field potentials. In turn, the MSs modulated both visually induced GBS and the speed of visually triggered behavioral responses. Fast/slow responses were preceded by a specific temporal pattern of MSs. These MS patterns induced perturbations in GBS that in turn explained variability in behavioral response speed. We hypothesize that the 3.3 Hz rhythm structures the sampling and exploration of the environment through building and breaking neuronal ensembles synchronized in the gamma-frequency band to process sensory stimuli.

Received March 11, 2009; revised May 14, 2009; accepted June 13, 2009.

Correspondence should be addressed to Dr. Conrado Bosman, Donders Institute for Brain, Cognition and Behaviour, Centre of Cognitive Neuroimaging, Radboud University Nijmegen, Kapittelweg 29, 6525 EN Nijmegen, The Netherlands. Email: c.bosman{at}donders.ru.nl






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