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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 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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“Accordingly, even though the relation between motor cortical oscillatory activity and the spiking activity of single neurons can be complex (Murthy and Fetz, 1996; Donoghue et al., 1998), it was found that there is a strong negative correlation between pyramidal neurons spiking rate and beta-band…”
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“In prior animal studies the narrow-band oscillations at or near 40 Hz, when present prior to action, tended to disappear when the animals become active in a behavioral task (Sanes and Donoghue, 1993; Oram et al., 1996; Murthy and Fetz, 1996; Kay and Freeman, 1998).”
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“…system (Laurent & Davidowitz 1994, Freeman 1972), in sensory and perceptual binding (Gray et al. 1989, Miltner et al. 1999, Rodriguez et al. 1999, Roelfsema et al. 1994, Singer & Gray 1995), in motor programming (Murthy & Fetz 1996), in associative learning (Buzsáki 2002, Larson & ∗Deceased.”
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“…binding process by providing a basis for unifying activity in the somatosensory and motor cortex during movement performance (Ribary et al. 1991; Murthy & Fetz 1992, 1996a,b; Sanes & Donoghue 1993), and in parietal areas engaged in perception with that in frontal areas engaged in planning…”
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“Likewise, the dramatic phase-shift at the lower border of layer 4, occurring both in vitro and in vivo (Murthy & Fetz, 1996), is consequently also a phenomenon arising within the isolated cortical network.”
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“Overall, our simulations, although obviously very simplified, are not incompatible with experimental observations in awake cats, monkeys, and humans, which indicates that oscillations do occur in awake animals and humans, particularly under conditions of focused, effortful processing, and are typically more prominent…”
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“In recent years, there has been a growing interest in the role of 42 neural oscillations in motor control (Baker et al., 1999; MacKay, 43 1997; Murthy and Fetz, 1996).”
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“For example, Murthy and Fetz reported that sites separated by up to 14 mm in precentral cortex showed significant correlation in the LFP activity in the 20–40 Hz band (Murthy and Fetz, 1996).”
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“, 2000), and with the attention paid (Murthy and Fetz, 1996; Kristeva-Feige et al., 2002).”
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“…a stable posture by inhibiting movement (Baker et al., 1999; Kü hn et al., 2008b), and the second that they are related to some aspect of movement planning or attention (Donoghue et al., 1998; Murthy and Fetz, 1992, 1996; Roux et al., 2006; Sanes and Donoghue, 1993; Schwartz et al., 2005).”
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“LFPs are not simply a reflection of neuronal spiking, but synchronization of spike timing to these oscillations occurs for some neurons in the sensorimotor and frontal cortex (Lebedev and Nelson, 1995; Murthy and Fetz, 1996b; Baker et al., 1999).”
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“Interestingly , epochs of high attention to motor performance ( and increased attention is very likely needed for successful learn - ing to control a BMI ) have been found to be associated with increases of synchrony between neurons ( Murthy and Fetz , 1992 , 1996a , b ; Riehle et al .”
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“We thank M. N. Franowicz who participated in some of the recordings, Y.-H. Liu for contribution to the initial phase of data analysis, and B. J. Pesaran for helpful comments on the manuscript.”
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“Murthy and Fetz (1996a) reported synchronous oscillations between sites within motor areas, between pre- and post-central sites and occasionally also between bilateral motor areas.”
BackgroundRole of the temporal domain for response selection and perceptual binding
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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
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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 229
“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
“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
“…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 215
Gaetz, W. C., & Cheyne, D. O. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.10.009 · Cited by 206
Synchronous oscillatory activity in sensory systems: new vistas on mechanisms
Ritz, R., & B, T. J. S. A. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80034-7 · Cited by 202
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 199
“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
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 192
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
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 197
Are Cortical Models Really Bound by the “Binding Problem”?
Riesenhuber, M., & Poggio, T. (1999) · Neuron · doi:10.1016/s0896-6273(00)80824-7 · Cited by 194
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 215
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 186
Manipulation of peripheral neural feedback loops alters human corticomuscular coherence
Riddle, C. N., & Baker, S. N. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.089607 · Cited by 185
“…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
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
“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 182
“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-citationIvry, R. B. (2000) · Human Brain Mapping · doi:10.1002/(sici)1097-0193(200003)9:3 · Cited by 73
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
“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
“…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
Metadata
- 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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