Neural Discharge and Local Field Potential Oscillations in Primate Motor Cortex During Voluntary Movements
Abstract
Donoghue, John P., Jerome N. Sanes, Nicholas G. Hatsopoulos, and Gyöngyi Gaál. Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J. Neurophysiol. 79: 159–173, 1998. The role of “fast,” or gamma band (20–80 Hz), local field potential (LFP) oscillations in representing neuronal activity and in encoding motor behavior was examined in motor cortex of two alert monkeys. Using chronically implanted microwires, we simultaneously recorded LFPs and single or multiple unit (MU) discharge at a group of sites in the precentral gyrus during trained finger force or reaching movements, during natural reaching and grasping, and during quiet sitting. We evaluated the coupling of oscillations with task-related firing at the same site, the timing of oscillations with respect to the execution of trained and untrained movement, and the temporal synchrony of oscillations across motor cortical sites. LFPs and neural discharge were examined from a total of 16 arm sites (7 sites in 1 monkey and 9 in the other), each showing movement-related discharge modulation and arm microstimulation effects. In the trained tasks, fast LFP and MU oscillations occurred most often during a premovement delay period, ceasing around movement onset. The decrease in oscillation roughly coincided with the appearance of firing rate modulation coupled to the motor action. During this delay, LFP oscillations exhibited either “overlapping” or “mixed” relationships with the simultaneously recorded neural discharge at that site. Overlap was characterized by coincident epochs of increased neural discharge and LFP oscillations. For the mixed pattern, episodes of LFP oscillation typically coincided with periods of diminished firing but overlap also sometimes appeared. Both patterns occurred concurrently across motor cortex during preparation; LFP suppression with motor action was ubiquitous. Fast oscillations reappeared quickly upon transition from quiet sitting to resumption of task performance, indicating an association with task engagement, rather than the general motor inaction of the delay period. In contrast to trained movements, fast oscillations often appeared along with movement during untrained reaching, but oscillations occurred erratically and were not reliably correlated with elevated neural discharge. Synchronous oscillations occurred at sites as much as 5 mm apart, suggesting widespread coupling of neurons and LFP signals in motor cortex. Widespread coupling of oscillatory signals is consistent with the concept that temporal coding processes operate in motor cortex. However, because the relationship between neuronal discharge and the appearance of fast oscillations may be altered by behavioral condition, they must reflect a global process active in conjunction with motor planning or preparatory functions, but not details of motor action encoded in neuronal firing rate.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Gamma power/spiking is anticorrelated with alpha/beta (8 to 30 Hz) power, which is higher under conditions of top-down control (e.g., attention and response inhibition).
“They are anticorrelated with alpha/beta (8 to 30 Hz) power (26–29), which is higher under conditions of top-down control (e.g., attention and response inhibition) (30–34).”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [32]
Cites
Plum, F. (1960) · Archives of Neurology · doi:10.1001/archneur.1960.03840090124020 · Cited by 10,388 · see citing works
Gray, C. M., König, P., Engel, A. K., & Singer, W. (1989) · Nature · doi:10.1038/338334a0 · Cited by 4,183 · see citing works
Visual Feature Integration and the Temporal Correlation Hypothesis
Singer, W., & Gray, C. M. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.003011 · Cited by 3,157 · see citing works
The representing brain: Neural correlates of motor intention and imagery
Jeannerod, M. (1994) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00034026 · Cited by 2,562 · see citing works
Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex
Gray, C. M., & Singer, W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.5.1698 · Cited by 2,463 · see citing works
Taussig, M. (1991) · Routledge eBooks · doi:10.4324/9780203397244 · Cited by 2,403 · see citing works
Coherent oscillations: A mechanism of feature linking in the visual cortex?
Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M., & Reitboeck, H. J. (1988) · Biological Cybernetics · doi:10.1007/bf00202899 · Cited by 2,329 · see citing works
Synchronization of cortical activity and its putative role in information processing and learning
Singer, W. (1993) · Annual Review of Physiology · doi:10.1146/annurev.ph.55.030193.002025 · Cited by 1,685 · see citing works
(1990) · CaltechAUTHORS (California Institute of Technology) · Cited by 1,661 · see citing works
High-frequency network oscillation in the hippocampus
Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. F., & Wise, K. D. (1992) · Science · doi:10.1126/science.1589772 · Cited by 1,223 · see citing works
A neural cocktail-party processor
von der Malsburg, C., & Schneider, W. (1986) · Biological Cybernetics · doi:10.1007/bf00337113 · Cited by 1,063 · see citing works
Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys.
Murthy, V. N., & Fetz, E. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.12.5670 · Cited by 996 · see citing works
Coherent 40-Hz oscillation characterizes dream state in humans.
Llinás, R., & Ribary, U. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.5.2078 · Cited by 962 · see citing works
Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement
Salmelin, R. H., & Hari, R. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90263-1 · Cited by 794 · see citing works
Synchronous oscillations in neuronal systems: Mechanisms and functions
Gray, C. M. (1994) · Journal of Computational Neuroscience · doi:10.1007/bf00962716 · Cited by 787 · see citing works
Johnson, P. B., Ferraina, S., Bianchi, L., & Caminiti, R. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.102 · Cited by 705 · see citing works
Computations Underlying the Execution of Movement: A Biological Perspective
Bizzi, E., Mussa-Ivaldi, F. A., & Giszter, S. F. (1991) · Science · doi:10.1126/science.1857964 · Cited by 681 · see citing works
Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation
Steriade, M., Amzica, F., & Contreras, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-01-00392.1996 · Cited by 646 · see citing works
The premotor cortex of the monkey
Weinrich, M., & Wise, S. P. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-09-01329.1982 · Cited by 618 · see citing works
Oscillations in local field potentials of the primate motor cortex during voluntary movement.
Sanes, J. N., & Donoghue, J. P. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.10.4470 · Cited by 583 · see citing works
Self-citationSpatial EEG patterns, non-linear dynamics and perception: the neo-sherringtonian view
Freeman, W. J., & Skarda, C. A. (1985) · Brain Research Reviews · doi:10.1016/0165-0173(85)90022-0 · Cited by 574 · see citing works
Murthy, V. N., & Fetz, E. E. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.6.3949 · Cited by 544 · cited 7× · see citing works
“…of single cellswith data from visual cortex that suggest a close link between stimulus-driven discharge and LFP oscillations at the same are mixed with aperiodic spiking (Murthy and Fetz 1996b). site (Eckhorn et al. 1988, 1993; Gray and Singer 1989; Gray et al. 1989; Kreiter and Singer 1992).”
BackgroundInfluentialMagnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans.
Ribary, U., Ioannides, A. A., Singh, K. D., Hasson, R., Bolton, J. P., Lado, F. A., Mogilner, A. Y., & Llinas, R. H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.24.11037 · Cited by 541 · see citing works
Synaptic background activity influences spatiotemporal integration in single pyramidal cells.
Bernander, Ö., Douglas, R. J., Martin, K. A. C., & Koch, C. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.24.11569 · Cited by 518 · see citing works
Shared Neural Substrates Controlling Hand Movements in Human Motor Cortex
Sanes, J. N., Donoghue, J. P., Thangaraj, V., Edelman, R. R., & Warach, S. J. (1995) · Science · doi:10.1126/science.7792606 · Cited by 470 · see citing works
Self-citationMurthy, V. N., & Fetz, E. E. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.6.3968 · Cited by 464 · see citing works
Richmond, B. J., Optican, L. M., Podell, M., & Spitzer, H. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.132 · Cited by 428 · see citing works
Direct physiological evidence for scene segmentation by temporal coding.
Engel, A. K., Peter König, B., & Singer, W. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.20.9136 · Cited by 399 · see citing works
Cognitive Neurophysiology of the Motor Cortex
Georgopoulos, A. P., Taira, M., & Lukashin, A. V. (1993) · Science · doi:10.1126/science.8465199 · Cited by 351 · see citing works
Oscillatory Neuronal Responses in the Visual Cortex of the Awake Macaque Monkey
Kreiter, A. K., & Singer, W. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00884.x · Cited by 333 · see citing works
Synchronization of oscillatory neuronal responses in cat striate cortex: temporal properties
Gray, C. M., Engel, A. K., König, P., & Singer, W. (1992) · Visual Neuroscience · doi:10.1017/s0952523800005071 · Cited by 317 · see citing works
Gray, C. M., Engel, A. K., Peter König, B., & Singer, W. (1990) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1990.tb00450.x · Cited by 315 · see citing works
Spatial properties of an EEG event in the olfactory bulb and cortex
Freeman, W. J. (1978) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(78)90126-8 · Cited by 313 · see citing works
Kristeva, R., Cheyne, D. O., & Deecke, L. (1991) · Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section · doi:10.1016/0168-5597(91)90015-p · Cited by 300 · see citing works
Bouyer, J. J., Montaron, M., & Rougeul, A. (1981) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(81)90138-3 · Cited by 256 · see citing works
Mitzdorf, U., & Singer, W. (1978) · Experimental Brain Research · doi:10.1007/bf00235560 · Cited by 250 · see citing works
High frequency (60–90 Hz) oscillations in primary visual cortex of awake monkey
Eckhorn, R., Frien, A., Bauer, R., Woelbern, T., & Kehr, H. (1993) · Neuroreport · doi:10.1097/00001756-199303000-00004 · Cited by 248 · see citing works
Simultaneous EEG 10 Hz desynchronization and 40 Hz synchronization during finger movements
Pfurtscheller, G., & Neuper, C. (1992) · Neuroreport · doi:10.1097/00001756-199212000-00006 · Cited by 210 · see citing works
Oscillatory discharge in the visual system: does it have a functional role?
Ghose, G. M., & Freeman, R. D. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.5.1558 · Cited by 196 · see citing works
Oscillatory firing and interneuronal correlations in squirrel monkey striate cortex
Livingstone, M. S. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.6.2467 · Cited by 194 · see citing works
Oscillatory activity is not evident in the primate temporal visual cortex with static stimuli
Tovée, M. J., & Rolls, E. T. (1992) · Neuroreport · doi:10.1097/00001756-199204000-00020 · Cited by 191 · see citing works
On oscillating neuronal responses in the visual cortex of the monkey
Young, M., Tanaka, K., & Yamane, S. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.6.1464 · Cited by 155 · see citing works
Anatomical localization of cortical beta rhythms in cat
Bouyer, J. J., Montaron, M., Vahnée, J. M., Albert, M. P., & Rougeul, A. (1987) · Neuroscience · doi:10.1016/0306-4522(87)92965-4 · Cited by 150 · see citing works
Rougeul, A., Bouyer, J. J., Dedet, L., & Debray, O. (1979) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(79)90205-0 · Cited by 149 · see citing works
Shadmehr, R., & Arbib, M. A. (1992) · Biological Cybernetics · doi:10.1007/bf00204111 · Cited by 140 · see citing works
Eckhorn, R. (1994) · Progress in brain research · doi:10.1016/s0079-6123(08)60556-7 · Cited by 134 · see citing works
Voltage-dependent fast (20–40 Hz) oscillations in long-axoned neocortical neurons
Núñez, Á., Amzica, F., & Steriade, M. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90464-d · Cited by 124 · see citing works
Temporal patterns of muscle activation for arm movements in three- dimensional space
Flanders, M. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-09-02680.1991 · Cited by 110 · see citing works
Roelfsema, P. R., Engel, A. K., Peter König, B., & Singer, W. (1996) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1996.8.6.603 · Cited by 106 · see citing works
Synaptic Interactions between Cortical Neurons
Fetz, E. E., Toyama, K., & Smith, W. S. (1991) · Cerebral cortex · doi:10.1007/978-1-4615-6622-9_1 · Cited by 101 · see citing works
Lopes, F. H. D. S., van Rotterdam, A., van Leeuwen, W. S., & Tielen, A. M. (1970) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(70)90138-0 · Cited by 97 · see citing works
Focused Arousal, 40-Hz EEG, and Dysfunction
Sheer, D. E. (1984) · Springer eBooks · doi:10.1007/978-3-642-69379-3_6 · Cited by 80 · see citing works
Single neurons are differently involved in stimulus-specific oscillations in cat visual cortex
Eckhorn, R., & Obermueller, A. (1993) · Experimental Brain Research · doi:10.1007/bf00229667 · Cited by 73 · see citing works
Montaron, M., Bouyer, J. J., Rougeul, A., & Buser, P. (1982) · Behavioural Brain Research · doi:10.1016/0166-4328(82)90010-9 · Cited by 69 · see citing works
Oscillatory neuronal activity related to visual short-term memory in monkey temporal pole
Nakamura, K., Mikami, A., & Kubota, K. (1992) · Neuroreport · doi:10.1097/00001756-199201000-00031 · Cited by 69 · see citing works
20 Hz rhythm of activity in visual system of perceiving cat.
Bekisz, M., & Wróbel, A. (1993) · PubMed · Cited by 45 · see citing works
Bauer, R., Brosch, M., & Eckhorn, R. (1995) · Brain Research · doi:10.1016/0006-8993(94)01273-k · Cited by 43 · see citing works
Synchronous Oscillations in Sensorimotor Cortex of Awake Monkeys and Humans
Murthy, V. N., Aoki, F., & Fetz, E. E. (1994) · Springer eBooks · doi:10.1007/978-1-4899-1307-4_24 · Cited by 21 · see citing works
Dynamic Motor Cortical Organization
Sanes, J. N., & Donoghue, J. P. (1997) · The Neuroscientist · doi:10.1177/107385849700300308 · Cited by 19 · see citing works
Self-citationCross Correlation Studies in Primate Motor Cortex: Event Related Correlation
Murphy, J. T., Kwan, H. C., & Wong, Y. C. (1985) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100046539 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dynamic predictions: Oscillations and synchrony in top–down processing
Engel, A. K., Fries, P., & Singer, W. (2001) · Nature Reviews Neuroscience · doi:10.1038/35094565 · Cited by 3,454 · see citing works
Neuronal ensemble control of prosthetic devices by a human with tetraplegia
Hochberg, L. R., Serruya, M. D., Friehs, G. M., Mukand, J. A., Saleh, M., Caplan, A. H., Branner, A., Chen, D., Penn, R. D., & Donoghue, J. P. (2006) · Nature · doi:10.1038/nature04970 · Cited by 3,295 · see citing works
Self-citationModulation of Oscillatory Neuronal Synchronization by Selective Visual Attention
Fries, P., Reynolds, J. H., Rorie, A. E., & Desimone, R. (2001) · Science · doi:10.1126/science.1055465 · Cited by 2,786 · see citing works
Neuronal Synchrony: A Versatile Code for the Definition of Relations?
Singer, W. (1999) · Neuron · doi:10.1016/s0896-6273(00)80821-1 · Cited by 2,581 · see citing works
Gamma and Beta Bursts Underlie Working Memory
Lundqvist, M., Rose, J., Herman, P., Brincat, S. L., Buschman, T. J., & Miller, E. K. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.028 · Cited by 846 · see citing works
Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics
Schwartz, A. B., Cui, X. T., Weber, D. J., & Moran, D. W. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.019 · Cited by 792 · see citing works
Miller, E. K., Lundqvist, M., & Bastos, A. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.023 · Cited by 797 · see citing works
Simeral, J. D., Kim, S.-P., Black, M. J., Donoghue, J. P., & Hochberg, L. R. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/2/025027 · Cited by 496 · see citing works
Self-citationvon der Malsburg, C. (1999) · Neuron · doi:10.1016/s0896-6273(00)80825-9 · Cited by 501 · see citing works
A network of electrically coupled interneurons drives synchronized inhibition in neocortex
Beierlein, M., Gibson, J. R., & Connors, B. W. (2000) · Nature Neuroscience · doi:10.1038/78809 · Cited by 489 · see citing works
Ritter, P., Moosmann, M., & Villringer, A. (2009) · Human Brain Mapping · doi:10.1002/hbm.20585 · Cited by 400 · see citing works
Oscillatory multiplexing of population codes for selective communication in the mammalian brain
Akam, T., & Kullmann, D. M. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3668 · Cited by 327 · see citing works
The Design of Integrated Circuits to Observe Brain Activity
Harrison, R. R. (2008) · Proceedings of the IEEE · doi:10.1109/jproc.2008.922581 · Cited by 330 · see citing works
Layer and rhythm specificity for predictive routing
Bastos, A. M., Lundqvist, M., Waite, A. S., Kopell, N., & Miller, E. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2014868117 · Cited by 268 · see citing works
Fast and Slow Oscillations in Human Primary Motor Cortex Predict Oncoming Behaviorally Relevant Cues
Saleh, M., Reimer, J., Penn, R., Ojakangas, C. L., & Hatsopoulos, N. G. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.001 · Cited by 281 · see citing works
Self-citationSelective 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
Neuronal coherence during selective attentional processing and sensory–motor integration
Womelsdorf, T., & Fries, P. (2006) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2007.01.005 · Cited by 156 · see citing works
Perelman, Y., & Ginosar, R. (2007) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2006.883732 · Cited by 116 · see citing works
Akam, T. E., & Kullmann, D. M. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002760 · Cited by 93 · see citing works
“Striking bursts of transient task dependent oscillatory activity are well documented in many brain regions including in motor cortex during movement preparation [32,33], the basal ganglia during cue utilization [34], and in visual cortex during working memory [35].”
BackgroundInhibitory motor control in response stopping and response switching
Kenner, N. M., Mumford, J. A., Hommer, R. E., Skup, M., Leibenluft, E., & Poldrack, R. A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1096-10.2010 · Cited by 92 · see citing works
Recording and decoding for neural prostheses
Warren, D. J., Kellis, S., Nieveen, J. G., Wendelken, S. M., Dantas, H., Davis, T. S., Hutchinson, D. T., Normann, R. A., Clark, G. A., & Mathews, V. J. (2016) · Proceedings of the IEEE · doi:10.1109/jproc.2015.2507180 · Cited by 52 · see citing works
- Authors
- Donoghue, J. P., Sanes, J. N., Hatsopoulos, N. G., & Gaál, G.
- Affiliations
- Brown University (US)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1998-01-01
- Volume
- 79
- Issue
- 1
- Pages
- 159-173
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1766529490
- Cited by
- 538
- References
- 60
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 5 · 2023: 10 · 2022: 13 · 2021: 14 · 2020: 16 · 2019: 17 · 2018: 18 · 2017: 19 · 2016: 17 · 2015: 14 · 2014: 20 · 2013: 16 · 2012: 19
- 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 (NS-25074)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- gamma oscillations, local field potentials, motor cortex, single-unit discharge, voluntary movement, motor preparation, temporal coding, reach-to-grasp, finger force, task engagement, motor planning
- MeSH terms
- Animals, Arcuate Nucleus of Hypothalamus, Brain Mapping, Electric Stimulation, Evoked Potentials, Macaca fascicularis, Motor Activity, Motor Cortex, Neurons, Oscillometry, Reaction Time, Muscle, Skeletal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
