High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex

The premotor cortex is well known for its role in motor planning. In addition, recent studies have shown that it is also involved in nonmotor functions such as attention and memory, a notion derived from both animal neurophysiology and human functional imaging. The present study is an attempt to bridge the gap between these experimental techniques in the human brain, using a task initially designed to dissociate attention from intention in the monkey, and recently adapted for a functional magnetic resonance imaging (fMRI) study [Simon, S.R., Meunier, M., Piettre, L., Berardi, A.M., Segebarth, C.M., Boussaoud, D. (2002). Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J. Neurophysiol., 88, 2047-57]. Intracranial EEG was recorded from the cortical regions preferentially active in the spatial attention and/or working memory task and those involved in motor intention. The results show that, among the different intracranial EEG responses, only the high gamma frequency (60-200 Hz) oscillatory activity both dissociates attention/memory from motor intention and spatially colocalizes with the fMRI-identified premotor substrates of these two functions. This finding provides electrophysiological confirmation that the human premotor cortex is involved in spatial attention and/or working memory. Additionally, it provides timely support to the idea that high gamma frequency oscillations are involved in the cascade of neural processes underlying the hemodynamic responses measured with fMRI [Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150-7], and suggests a functional selectivity of the gamma oscillations that could be critical for future EEG investigations, whether experimental or clinical.

[1]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[2]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[3]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[4]  A. Dale,et al.  Coupling of Total Hemoglobin Concentration, Oxygenation, and Neural Activity in Rat Somatosensory Cortex , 2003, Neuron.

[5]  T. Allison,et al.  Linking hemodynamic and electrophysiological measures of brain activity: evidence from functional MRI and intracranial field potentials. , 2004, Cerebral cortex.

[6]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[7]  J. Bouyer,et al.  Fast somato-parietal rhythms during combined focal attention and immobility in baboon and squirrel monkey. , 1979, Electroencephalography and clinical neurophysiology.

[8]  Arthur W. Toga,et al.  Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex , 2004, The Journal of Neuroscience.

[9]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[10]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[11]  D. Boussaoud Attention versus Intention in the Primate Premotor Cortex , 2001, NeuroImage.

[12]  Dae-Shik Kim,et al.  Spatial relationship between neuronal activity and BOLD functional MRI , 2004, NeuroImage.

[13]  S. P. Wise,et al.  Primate frontal cortex: neuronal activity following attentional versus intentional cues , 2004, Experimental Brain Research.

[14]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[15]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[16]  D. Boussaoud,et al.  Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. , 2002, Journal of neurophysiology.

[17]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[18]  Martin Lauritzen,et al.  Brain Function and Neurophysiological Correlates of Signals Used in Functional Neuroimaging , 2003, The Journal of Neuroscience.

[19]  A. Toga,et al.  Linear and Nonlinear Relationships between Neuronal Activity, Oxygen Metabolism, and Hemodynamic Responses , 2004, Neuron.

[20]  S. P. Wise,et al.  Primate frontal cortex: effects of stimulus and movement , 2004, Experimental Brain Research.

[21]  G. Pfurtscheller Central beta rhythm during sensorimotor activities in man. , 1981, Electroencephalography and clinical neurophysiology.

[22]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[23]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[24]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[25]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[26]  Andrea Brovelli,et al.  Medium-Range Oscillatory Network and the 20-Hz Sensorimotor Induced Potential , 2002, NeuroImage.

[27]  Conrad V. Kufta,et al.  Event-related desynchronization and movement-related cortical potentials on the ECoG and EEG. , 1994, Electroencephalography and clinical neurophysiology.

[28]  S. Wise,et al.  Tuning for the orientation of spatial attention in dorsal premotor cortex , 2001, The European journal of neuroscience.

[29]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Hari,et al.  Synchronous cortical oscillatory activity during motor action , 2003, Current Opinion in Neurobiology.

[31]  R. Hari,et al.  Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement , 1994, Neuroscience.

[32]  R P Lesser,et al.  Functional significance of the mu rhythm of human cortex: an electrophysiologic study with subdural electrodes. , 1993, Electroencephalography and clinical neurophysiology.

[33]  A. Grace,et al.  Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior , 2005, Nature Neuroscience.

[34]  William A. MacKay,et al.  Field potential oscillatory bursts in parietal cortex before and during reach , 1995, Brain Research.

[35]  J. Donoghue,et al.  Oscillations in local field potentials of the primate motor cortex during voluntary movement. , 1993, Proceedings of the National Academy of Sciences of the United States of America.