Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior
Abstract
1. Oscillations of 20-40 Hz were observed in local field potentials (LFPs) and unit activity in sensorimotor cortices of three awake monkeys while the monkeys performed trained wrist movements and untrained exploratory arm movements. The mean frequency of LFP oscillations was 25.9 +/- 1.4 (SD) Hz and the number of cycles of oscillations per episode was variable, with a mean of 4.2 +/- 0.5 (mean +/- SE). 2. Oscillatory episodes occurred most often when the monkeys retrieved raisins from a Klüver board (0.59 +/- 0.23 episodes per s, mean +/- SD) or from unseen locations with the use of somatosensory feedback (0.62 +/- 0.12 episodes per s); they occurred less often when the monkeys performed repetitive wrist flexion and extension movements (0.22 +/- 0.04 episodes per s) or sat quietly at rest (0.23 +/- 0.17 episodes per s). 3. The amplitude of LFP oscillations increased with depth in cortex, reaching a maximum between 1 and 2 mm. LFP oscillations at the surface of the cortex were 180 degrees out of phase with oscillations in the deep cortical layers. The phase shift (with respect to the deep layers) decreased with depth in the cortex and disappeared at depths of > 1 mm. 4. LFPs were recorded simultaneously at multiple sites in the sensorimotor cortex when monkeys retrieved raisins from a Klüver board or from unseen locations. Cross-correlation of LFPs recorded at different sites indicated that oscillations in the 20- to 40-Hz range could become synchronized at sites separated by up to > or = 14 mm in the precentral cortex. 5. The probability of occurrence of significant correlations between LFP oscillations at paired sites and the average correlation amplitude decreased with increasing horizontal separation of sites in precentral cortex. The phase shift between LFP oscillations recorded at paired sites did not change significantly with increasing horizontal separation. 6. For paired sites in precentral cortex, the average strength of correlations and the proportion of oscillations that were significantly correlated were greater during exploratory behaviors such as retrieving raisins from slots of the Klüver board than during periods of rest or overtrained wrist movements. 7. Oscillations could become synchronized with small phase shifts (0.5 +/- 1.6 ms) between pre- and postcentral cortical sites. Average strength and probability of occurrence of significant correlations between pre- and postcentral LFPs increased during exploratory behaviors. 8. Oscillations occurred simultaneously in the left and right motor cortex and could become synchronized with negligible phase shifts when the monkey performed bimanual manipulations. However, synchronization occurred as often and as strongly for unimanual as for bimanual manipulations. 9. These results indicate that episodes of 20- to 40-Hz oscillations occur often and become synchronized over a large cortical area during exploratory forelimb movements. However, they have no reliable relation to particular components of the movement and therefore seem unlikely to be involved directly in movement execution; instead, they may represent a neural correlate of attention during demanding sensorimotor behaviors.
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Locomotion is associated with a simultaneous increase in 30-80 Hz gamma band activity.
“Locomotion is also associated with a simultaneous increase in 30–80 Hz gamma band activity.”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Murthy and Fetz, 1996
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“Similar evidence is available for the motor system, where neural synchronization in the gamma frequency range has been discovered in cats (Steriade et al., 1996), monkeys (Murthy and Fetz, 1992, 1996a,b; Sanes and Donoghue, 1993) and humans (Kristeva-Feige et al., 1993).”
BackgroundInfluentialIonic Mechanisms Underlying Repetitive High-Frequency Burst Firing in Supragranular Cortical Neurons
Brumberg, J. C., Nowak, L. G., & McCormick, D. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-04829.2000 · Cited by 234 · see citing works
Multiple Features of Motor-Unit Activity Influence Force Fluctuations During Isometric Contractions
Taylor, A. M., Christou, E. A., & Enoka, R. M. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00056.2003 · Cited by 233 · see citing works
Neural mechanisms of mental fatigue
Ishii, A., Tanaka, M., & Watanabe, Y. (2014) · Reviews in the Neurosciences · doi:10.1515/revneuro-2014-0028 · Cited by 237 · see citing works
The role of GABAergic modulation in motor function related neuronal network activity
Hall, S. D., Stanford, I. M., Yamawaki, N., McAllister, C. J., Rönnqvist, K. C., Woodhall, G. L., & Furlong, P. L. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.02.025 · Cited by 215 · see citing works
“At rest, the primary motor cortex (M1) exhibits ongoing neuronal network oscillations in the beta (15-30Hz) frequency range (Baker et al., 1997; Murthy and Fetz, 1996).”
Baker, S. N., Pinches, E. M., & LEMON, R. N. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00832.2002 · Cited by 214 · see citing works
“Murthy and Fetz (1996b) showed explicitly an increase in pairwise neuronal synchrony during epochs of field potential oscillatory activity.”
BackgroundMethodResultInfluentialGoldberg, J. A., Rokni, U., Boraud, T., Vaadia, E., & Bergman, H. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4848-03.2004 · Cited by 211 · see citing works
“…that were separated by up to a few millimeters in either cortex or the BG, indicating that the LFPs constitute a signal common to large volumes of tissue (Eckhorn and Obermueller, 1993; Sanes and Donoghue, 1993; Murthy and Fetz, 1996b; Contreras et al., 1997; Bullock, 1999; Destexhe et al., 1999).”
BackgroundResultInfluentialMovement-related change of electrocorticographic activity in human supplementary motor area proper
Ohara, S. (2000) · Brain · doi:10.1093/brain/123.6.1203 · Cited by 209 · see citing works
Gaetz, W. C., & Cheyne, D. O. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.10.009 · Cited by 206 · see citing works
Synchronous oscillatory activity in sensory systems: new vistas on mechanisms
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Accurate decoding of reaching movements from field potentials in the absence of spikes
Flint, R. D., Lindberg, E. W., Jordan, L. R., Miller, L. E., & Slutzky, M. W. (2012) · Journal of Neural Engineering · doi:10.1088/1741-2560/9/4/046006 · Cited by 202 · see citing works
“1741-2560/12/046006+13$33.00 1 © 2012 IOP Publishing Ltd Printed in the UK & the USA”
InfluentialSynchronized neuronal oscillations and their role in motor processes
MacKay, W. A. (1997) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(97)01059-0 · Cited by 202 · see citing works
Coding and transmission of information by neural ensembles
Averbeck, B. B., & Lee, D. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.02.006 · Cited by 190 · see citing works
Baker, S. N., Spinks, R. L., Jackson, A., & Lemon, R. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.2.869 · Cited by 198 · see citing works
The Psychophysical Evidence for a Binding Problem in Human Vision
Wolfe, J. M., & Cave, K. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)80818-1 · Cited by 194 · see citing works
Are Cortical Models Really Bound by the “Binding Problem”?
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Brain Oscillations in Sport: Toward EEG Biomarkers of Performance
Cheron, G. A., Petit, G., Chéron, J., Leroy, A., Cebolla, A. M., Cevallos, C., Petieau, M., Hoellinger, T., Zarka, D., Clarinval, A.-M., et al. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00246 · Cited by 197 · see citing works
Neurophysiologic correlates of fMRI in human motor cortex
Hermes, D., Miller, K. J., Vansteensel, M. J., Aarnoutse, E. J., Leijten, F. S. S., & Ramsey, N. F. (2011) · Human Brain Mapping · doi:10.1002/hbm.21314 · Cited by 185 · see citing works
Manipulation of peripheral neural feedback loops alters human corticomuscular coherence
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“…much recent interest in motor cortical oscillations, where rhythms at ∼10 Hz and ∼15–30 Hz occur in both animals and humans (Salmelin & Hari, 1994; Murthy & Fetz, 1996; Stancak & Pfurtscheller, 1996; Baker et al. 1997; Salenius et al. 1997; Donoghue et al. 1998; Halliday et al. 1998; Brown et…”
BackgroundSelective inhibition of movement
Coxon, J. P., Stinear, C. M., & Byblow, W. D. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01284.2006 · Cited by 173 · see citing works
The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man
Baker, M. R., & Baker, S. N. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.029553 · Cited by 180 · see citing works
“Oscillations around 20–30 Hz (‘beta’ band) arise from the primary motor cortex (Murthy & Fetz, 1996; Baker et al. 1997; Donoghue et al. 1998; Kilner et al. 1999).”
BackgroundIncreased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks
Aoki, F., Fetz, E. E., Shupe, L., Lettich, E., & Ojemann, G. A. (1999) · Clinical Neurophysiology · doi:10.1016/s1388-2457(98)00064-9 · Cited by 177 · see citing works
“The cortical extent of the synchronous activity was more restricted in these human recordings than previously found in monkey sensorimotor cortex (Bressler et al., 1993; Murthy and Fetz, 1992; Murthy and Fetz, 1996a; Sanes and Donoghue, 1993).”
InfluentialSelf-citationAnticipatory cerebellar responses during somatosensory omission in man
Tesche, C. D., & Karhu, J. (2000) · Human Brain Mapping · doi:10.1002/(sici)1097-0193(200003)9:3 · Cited by 176 · see citing works
Lau, D., de Miera, E. V., Contreras, D., Ozaita, A., Harvey, M., Chow, A., Noebels, J. L., Paylor, R. E., Morgan, J. I., Leonard, C. S., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09071.2000 · Cited by 175 · see citing works
“As shown in Figure 11 A , wild-type mice ( n 5 21) showed the characteristic slow rhythm observed during natural slow-wave sleep and during ketamine–xylazine anesthesia in other species (Steriade et al., 1993a; Contreras and Steriade, 1995).”
Changes in corticospinal drive to spinal motoneurones following visuo‐motor skill learning in humans
Pérez, M. A., Lundbye‐Jensen, J., & Nielsen, J. B. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.105361 · Cited by 174 · see citing works
“…corticospinal input to spinal motoneurones have been shown to take place during a motor task that requires a high degree of attention and precision (Murthy & Fetz, 1996; Schmied et al. 2000; Kilner et al. 2002; Kristeva-Feige et al. 2002), but, so far, the interaction between corticospinal inputs…”
BackgroundThe response of cat visual cortex to flicker stimuli of variable frequency
Rager, G. H., & Singer, W. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00197.x · Cited by 170 · see citing works
- Authors
- Murthy, V. N., & Fetz, E. E.
- Affiliations
- University of Washington (US)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1996-12-01
- Volume
- 76
- Issue
- 6
- Pages
- 3949-3967
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1787747564
- Cited by
- 544
- References
- 0
- Citations by year
- 2026: 4 · 2025: 12 · 2024: 11 · 2023: 11 · 2022: 13 · 2021: 13 · 2020: 13 · 2019: 11 · 2018: 16 · 2017: 16 · 2016: 16 · 2015: 16 · 2014: 25 · 2013: 17 · 2012: 18
- FWCI
- 14.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS12542)
- National Center for Research Resources (RR00166, P51RR000166)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- sensorimotor cortex, local field potentials, cortical oscillations, neuronal synchronization, precentral cortex, inter-site correlation, exploratory behavior, somatosensory feedback, arm movement, monkey behavior, unit activity
- MeSH terms
- Animals, Electromyography, Evoked Potentials, Somatosensory, Exploratory Behavior, Feedback, Hand, Functional Laterality, Macaca mulatta, Macaca nemestrina, Movement, Neurons, Periodicity, Somatosensory Cortex, Time Factors, Evoked Potentials, Motor
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