Proc. Natl. Acad. Sci. USAVol. 90, pp. 4470-4474, May 1993Neurobiology

Oscillations in local field potentials of the primate motor cortexduring voluntary movement

(neural oscillations/local neural drcults/insructd voluntary movements/forearm/monkeys)

JEROME N. SANES AND JOHN P. DONOGHUEDepartment of Neuroscience, Division of Biology and Medicine, Brown University, Providence, RI 02912

Communicated by Francis Crick, January 15, 1993 (receivedfor review November 5, 1992)

ABSTRACT We investigated the occurrence and distribu-tion of oscillator activity in local field potentials (LFPs)recorded from the frontal motor cortex of behaving monkeysperforming skilled voluntary movements. LFPs were recordedsimultaneously from up to 12 sites distributed throughoutmotor cortex while monkeys performed a visually guided,instructed delay task using the wrist or digits. Oscillatoryactivity between 15 and 50 Hz was evident in the LFP recordedfrom both primary motor cortex and premotor areas. Oscil-lations occurred preferentially before the visual cue to initiatemovement but were infrequent during movement. Oscilationstypically stopped before movement initiation during the wristtask, although they often continued into the initial phases ofmovement during the digit task. The relationship of oscillationsto task performance was consistent across trils over periods ofmany months, although the amplitude and duration of oscil-lations varied across trials and days. Interactions between pairsof LFP recordings, evaluated with cross-correlation analysis,revealed synchronous oscillations over long distnces (>7 mm)and across primary motor cortex and premotor recording sites.These studies demonstrate that oscillations recorded in the LFPin motor cortex during trained motor tasks are not related tothe details ofmovement execution but may be related to aspectsof movement preparation.

Oscillatory activity of single neurons, of multiunit activity,and of local field potentials (LFPs) in the 20- to 50-Hz rangeoccurs in a variety of cerebral cortical structures includingmammalian olfactory (1), visual (2-6), somatic sensory (7),and motor (8-10) cortex. Oscillations in LFPs or multiunitactivity obtained from visual cortex (3) may reflect synchro-nized activity of local neuron assemblies related to informa-tion processing in these areas. Further investigations haverevealed synchronization of multiunit oscillations in homol-ogous regions of visual cortex in the two hemispheres (11)and in separate areas of visual cortex within one hemisphere(12). Correlation of neural activity in widely separated visualcortical areas may be a neural implementation of featurebinding that could produce unified perception of a complexsensory stimulus (13, 14).A number of cerebral cortical areas are closely related to

planning and performing voluntary movement (15). The pri-mary motor cortex (MI) is most closely tied to aspects ofexecution, whereas premotor areas appear to have a greaterrole in motor planning. Neural oscillations in cortical motorareas could reflect specific aspects of activity related tomotor planning and performance or to sensory input. Oscil-latory rhythms in field potentials have long been known toexist in motor cortical areas (16). They have been associatedwith aspects of attention and with movement. In cats andmonkeys, "fast rhythms" reportedly occur during attentive

states and terminate with movement (16), but more recently,Murthy and Fetz (9) reported the occurrence of LFPs andunit oscillations in the 25- to 35-Hz range in MI whilemonkeys performed arm movements. These workers notedthat oscillations occurred more frequently during free reach-ing, especially when the animals reached for objects outsidethe visual field. Oscillations occurred less frequently duringrepetitive movements or during immobility. However, noneof the previous studies used motor tasks that permitted anassessment of how neural oscillations in motor cortex relateto features of attentiveness, preparation, and performanceoccurring in a learned motor task. Furthermore, previousstudies concerning neural oscillations in motor cortex typi-cally recorded activity from single sites; the synchronizationof activity across motor cortical areas during preparation andexecution of movement was not assessed. In the currentexperiments, we examined LFPs recorded simultaneouslyfrom up to 12 sites across MI and premotor area (PMA) whilemonkeys performed wrist or digit movements in a visuallyguided, step-tracking task with an instructed delay. We foundthat 15- to 50-Hz oscillations in the LFPs were most prom-inent before movement onset, but their onset time was notcorrelated with occurrence ofinstructional cues. By contrast,the cessation of LFP oscillations was correlated over wideareas with movement onset. Oscillations were correlatedbetween sites related to different joints of the arm and indifferent subdivisions of the frontal motor cortex. Thestrength of correlation had no relationship to the distancebetween recording sites.

MATERIALS AND METHODSTwo male monkeys (Macaca fascicularis) weighing 4-5 kgused visual cues in an instructed delay task either to performwrist flexion movements or downward-directed finger flexorforce. The animals sat in a primate chair positioned in frontof a computer-controlled video screen with the right forearmgently restrained. For wrist movements, the hand was placedbetween two padded plates with the wrist coaxial with theaxis of a torque motor. Wrist movements were performedagainst a mild spring load, and a video screen displayedtargets for the monkey to acquire by positioning a cursorrepresenting wrist angle. For each trial, the monkeys posi-tioned the hand at 15° ofwrist flexion for 3-4 sec. After 1-2sec of holding without instructions (the hold period), apre-cue target appeared for 2-3 sec on the video screen toinstruct the location of the upcoming 250 or 450 flexionmovement (the pre-cue period). The monkey was instructedto move when the go-cue target changed appearance. For thedigit task, the monkey held the right hand on a plate mountedto a strain gauge using the same visual cues as for the wristtask. The initial force was minimal or zero, and the new forcetarget was signaled by a pre-cue. The monkey was required

Abbreviations: LFPs, local field potentials; MI, primary motorcortex; PMA, premotor area.

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The publication costs of this article were defrayed in part by page chargepayment. This article must therefore be hereby marked "advertisement"in accordance with 18 U.S.C. §1734 solely to indicate this fact.

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Proc. Natl. Acad. Sci. USA 90 (1993) 4471

to attain a new wrist position or digit force within 1 sec of thego cue and to hold the new position or force for 500 msec toreceive a liquid reinforcement.

After the monkeys consistently received liquid on 85% ofthe trials, recording wires were surgically implanted in themotor cortex using sterile procedures and inhalant anesthesia(Isoflurane). Monkeys were mounted in a stereotaxic instru-ment, and a craniotomy was made over the motor cortex. Thedura mater was resected, and up to 25 wires (50-j.m diameterPtIr wire, coated with 10-,um Teflon) were inserted into thecortex between the central and arcuate sulci and to depthsconsistent with layer V. After insertion of all wires, the set ofelectrodes and the cortical surface were covered first withFibrin glue (Immuno US, New York), and then the entireassembly, including anchor screws and a connector, wascovered with dental acrylic.

Neural Activity Recording and Analysis. A 25-channel head-stage preamplifier (Microprobe, Clarksburg, MD) wasmounted directly on the monkey's head. The headstageoutput was led to Grass Instruments AC-coupled amplifiersand then to a 16-channel Vetter videotape signal conditioner.For further categorization of recording sites, the cortex wasstimulated with trains of stimuli (333-Hz trains, 30-msecduration, 200-,usec pulses) using currents up to 60 AA.For analysis of the LFPs relationship to behavior, hand

position or digit force and up to 12 channels of neural datawere digitized from videotape at 2.5 kHz (LFP-filtered at10-100 Hz, 3 decibel points) and in epochs of 6.6 sec,beginning at the onset of each movement cycle. The LFPswere low-pass filtered digitally (flat region = 0-52 Hz; 3decibel point = 62 Hz; 20 decibels down at 70 Hz). Thefrequency spectrum for each waveform was derived withstandard fast Fourier transforms, and a sliding spectrogram(256-msec epochs, 25-msec steps) between 15-45 Hz in 5-Hzbands was computed. Auto- and cross-correlograms andsliding (256-msec epochs, 50-msec steps) auto- and cross-correlograms were computed.

RESULTSMonkey FC was studied over an 18-mo period. Of 17 wiresimplanted in motor cortex, electrical stimulation evokedcontralateral arm movements at 11 sites; the remaindershowed head or leg movements or no effect. Recordings wereobtained from 14 sites. Monkey FD, studied for 6 mo, had 25implanted wires. Movements were evoked by stimulating 23wires; arm movements were evoked at 17 sites, whereasrecordings were obtained from 18 wires.

Microwire Location. Histological evaluation of wire place-ment is currently unavailable because the two monkeys fromwhich neural activity reported upon in this paper was ob-tained are still participating in experiments. From surfacereconstruction of wire placement obtained during implanta-tion and the electrical stimulation results, it would appearthat most wires are located in the MI arm area or in area 6immediately posterior and medial to the genu of the arcuatesulcus, commonly termed PMA.General LFP Characteristics. LFPs recorded at most motor

cortex sites exhibited oscillatory activity (Fig. 1). In monkeyFC, oscillations did not occur at a MI leg site, and they wereweak at one MI wrist site and at two PMA sites related toneck and head movement. Oscillations in monkey FD oc-curred at leg sites but were weak at three MI wrist and digitsites. There was no obvious difference in the presumedlocation or depth of nonoscillating and oscillating sites.Oscillations were similar for FC and FD at topographicallydifferent locations within MI and PMA. LFP oscillationscould be episodic or sustained, and durations of severalseconds were evident. The longest sustained period of oscil-lation endured throughout the 6- to 8-sec period of the

\ Hand Position

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FIG 1. LFPs during instructed delay task. LF PMAr Wrist (w6)

movemen. The tp recor displas hand ositio anduthe LFP

recorded from eachMI and PMAsite.EachrecornPMA: Leg (w18)

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FIG. 1. LFPs during instructed delay task. LFP recordings from11 wires implanted in motor cortex of monkey FD during a wristmovement. The top record displays hand position and the LFPrecorded from each MI and PMA site. Each recording is identifiedwith the low threshold movement evoked by intracortical electricalstimulation and an identification code. Note the diversity of LFPoscillations in the various records, from relatively briefbursts ofLFPsynchrony (wire 18, from 3 to 4 sec) to sustained synchrony in severalrecordings (e.g., wires 7, 8, and 16). Note that oscillations and highamplitude diminish after the go cue and remain suppressed through-out the hand movement. (LFP calibration = 100 pV.)

instructed delay task, although waxing and waning of ampli-tude were observed during such episodes.

Fig. 2 illustrates multiple examples of LFPs obtained fromone site examined across nearly 15 mo when monkey FCperformed either the wrist (Ai-A5 and B1-B2) or digit (C,-C3)task. As shown here, the duration, magnitude, and precisetime of occurrence of the oscillations varied somewhat fromtrial to trial and day to day. Threshold electrical stimulationat this MI site evoked thumb extension and wrist extension.

Occurrence of LFP During Tasks. Oscillations showedcertain consistent relationships to behavior across the twomonkeys and two tasks (Figs. 1-3A, 4B). At most record-ing sites, oscillations were most pronounced during the holdand pre-cue periods. The oscillations declined markedlyaround movement onset and remained suppressed during themovement. There was a noteworthy difference in the timingof cessation of LFP oscillatory activity for the two tasks.Although obvious oscillations generally ceased before wrist-movement onset, they often continued for a short time afteronset of digit force (compare traces in Fig. 2 A and B withthose in C). Oscillations rarely occurred during the dynamicphase of wrist movement, although they sometimes reap-peared during the subsequent static hold; at this time theoscillations were usually of lower amplitude and shorterduration than observed before movement onset (right sec-tions of Fig. 1). For both tasks, oscillations were againprominent when the monkey returned to the holding positionto begin the next trial. The pre-cue, which signaled the extent

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4472 Neurobiology: Sanes and Donoghue

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FIG. 2. Reproducibility ofLFP oscillations. Recordings from onewire implanted in MI of monkey FC and kinematic records (upper ofpair) obtained during seven wrist movements (A and B) and threedigit motor actions (C). All records are aligned on movement onsetwith the go-cue onset indicated by the downward pointing triangle.(A) Records from a set of 100 trials when the monkey performedsingle-amplitude wrist-flexion movements. (B) Records from a re-cording session 2 days earlier (B,) and one session 6 days later (B2)than those in A but while the monkey performed either shorter orlonger wrist movements. (C) A record from each of 3 days >1 yr laterthan those from A and B but while the monkey worked in the digittask. For all records, the LFP oscillations were most evident beforethe go cue and declined either before movement onset (wrist) or inthe early stages of movement (digit). (LFP calibration = 100 AV.)

of the upcoming movement, appeared =2 sec later. In thevast majority of cases there was no striking change in theappearance of oscillations before or after the pre-cue ap-peared. Thus, there was no strict temporal correlation be-tween visual cues and oscillatory episodes. It is also note-worthy that, although task conditions varied in the hold andpreparatory periods (i.e., regarding visual cueing), there wasno obvious or consistent manifestation in the monkey'sbehavior that indicated a change in set or attention betweenthese two premovement periods. Despite the visual cueing,the monkey sometimes failed to perform, and oscillationsduring these trials typically continued until the next move-ment sequence.

Similar to observations by others in visual cortex (3) andMI (9), the frequency of LFP oscillations was in the 15- to50-Hz range. The dominant frequencies differed for the twomonkeys. In initial recordings from monkey FC, the domi-nant frequency clustered around 28 Hz, whereas that formonkey FD clustered around 20-25 Hz. When monkey FCswitched from the wrist to the digit task, the dominantfrequency clustered around 35 Hz, but no similar frequencyshift occurred in monkey FD. Presently, we do not know whyoscillation frequency during the digit task was higher only inmonkey FC.During a single trial, the dominant frequency of oscillations

was similar across wires. However, peak frequency varia-tions of a few Hz occurred between different trials, althoughthis variation had no evident relationship to active motorbehavior. By contrast, frequency spectrograms in 5-Hzbands between 15 and 45 Hz revealed subtle differences in thewaxing and waning offrequency across recording sites during

a trial (Fig. 3). At some sites, LFP frequency modulation wasmost evident within a relatively narrow bandwidth, suggest-ing that different forms of information could be carried overrestricted frequency ranges in the LFP.

Cortical Interactions. We used cross-correlation methodsto examine relationships of oscillatory activity occurringsimultaneously at various recording sites. Fig. 4 illustrates"correlograms" calculated for LFP recorded at five motorcortex sites during one wrist movement. Each of these siteswas classified either as a digit or a wrist site, according to theelectrical stimulation effects. Two types of interactions aredepicted. First, the insets above the right side of eachhistogram show the cross- or auto-correlograms computedwhile the monkey performed one wrist movement. Thecorrelograms indicated a range of interactions from absenceof interaction (data not shown) to a high degree of synchrony.We found that the strength ofcorrelation did not depend uponpropinquity of recording sites. Oscillations occurring in twosites distant from each other, even in different cortical motorareas, could be highly correlated. For example, activity atsite 7 in PMA, a "thumb" site, and site 8 in MI, a "thumb andwrist" site, was highly correlated, even though the sites wereseparated by more than 3 mm (measured along the corticalsurface) and had different evoked movement effects. Bycontrast, wires 7 and 13 were separated by 1.6 mm, but theiroscillations were less strongly correlated.A second analysis correlated activity between pairs ofLFP

recordings in successive 256-msec epochs stepped at 50 msecacross the entire behavioral period (histograms in Fig. 4A).LFPs recorded at several pairs ofmotor cortical sites showed

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FIG. 3. Frequency characteristics of motor cortex LFPs. (A)Recordings from MI and PMA during a single trial performed bymonkey FD. The cued preparatory period occurred between thedashed lines, and go-cue onset is indicated by the rightmost dashedline. (LFP calibration = 100 ,uV.) (B) Cumulative amplitude of theFourier decomposition of the LFP recordings in 5-Hz bandwidthsfrom 15 to 45 Hz calculated in 256-msec epochs and stepped acrossthe trial in 25-msec increments. Note that the power in the threebands from 15 to 30 Hz exhibited the greatest spectral density beforemovement and the most diminution of power during active move-ment.

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Proc. Natl. Acad. Sci. USA 90 (1993) 4473

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FIG. 4. Interactions between corticalsites. (A) Auto- and cross-correlation ma-trix of a selected set of LFP recordingsduring a single wrist movement (dis-played under histogram in upper right)performed by monkey FD. (Insets aboveright sections) The auto- (on matrix diag-onal) or cross-correlogram of the record-ing pairs computed across the entire be-havioral trial; only the central portion ofthese records is shown. Each histogrambin represents the peak value ofauto- andcross-correlograms ofshort epochs acrossthe behavioral trial (see text for details).(Correlogram calibration for entire epoch= 0.05; calibration for sliding correlo-grams = 0.1.) (B) LFP recordings fromeach site depicted in A. (LFP calibration= 100 uV.)

high peak correlations in the hold and pre-cue periods butwith significant fluctuations, and decreased correlation atmovement onset, reflecting the cessation of the high-amplitude oscillatory activity. Although there was consider-able variability in the time of onset and duration of oscilla-tions from trial to trial, the pattern of strong correlationbetween wire pairs in the hold and pre-cue period was

observed across trials (data not shown).

DISCUSSIONThese results demonstrate that widespread synchronous os-cillatory activity occurs in motor cortex during preparationfor visually guided movements. The cessation of oscillatoryactivity occurs simultaneously across motor cortex at move-ment onset. Thus, these results confirm prior observationsthat LFP oscillations occur in motor cortex of behavingmonkeys (9) and demonstrate spatiotemporal features ofneural oscillatory activity occurring during preparation andperformance of learned movements to visual targets. Oscil-lations occurred predominantly in the uncued (hold) and cuedintervals before visual signals instructed hand motor actions.These oscillations were markedly damped after the go cueand during the dynamic phase of movement, although theycould continue into the initial part of digit movements.Across trials and in both monkeys, oscillations in the LFP

occurred consistently throughout the hold and pre-cue peri-ods, although the exact pattern of oscillations varied fromshort bursts (one cycle or -25-50 msec) to nearly continuousperiods lasting for several seconds. These findings differ fromthose of Murthy and Fetz (9), who found LFP oscillations inMI occurring in five-cycle bursts and at very low rates(<1/sec) when monkeys performed repetitive wrist move-ments. In the current experiment, monkeys performed avisually guided step-tracking task requiring precise flexion toa defined target, and LFP oscillations appeared frequentlyand sometimes continuously throughout the period leadingup to movement. A potential reason for the discrepancy in theoccurrence of LFP oscillations between our experiment andthat of Murthy and Fetz (9) may be differences in theconditions directing the monkeys' behavior, the precision of

the tasks, or when oscillatory activity was evaluated. Ourexperiments used a more complex step-tracking task thatincluded an instructed delay period during which impendingtarget location could be seen by the monkey, whereas thebehavioral contingencies of Murthy and Fetz (9) apparentlydid not always require target visualization. Regardless ofthese differences both studies find infrequent LFP oscilla-tions during actual performance of overtrained movements.Our data support earlier findings from cat (8) and monkey

(9, 16) that motor cortex LFP oscillations may be related toattentive states. However, we found no readily apparentrelationship between the occurrence or duration of LFPoscillations and onset of instruction cues, which would beexpected to increase attentiveness. This finding may berelated to our inability to measure or to control attentivenessprecisely in the hold or pre-cue periods. Nevertheless, shortand consistent reaction times suggest that the monkey main-tained a high level of attention during the variable-lengthinstructed delay period.The most notable temporal relationship ofLFP oscillations

to behavior was the marked desynchronization and amplitudediminution after the go cue occurred. At this time, move-ment-related unit activity begins in motor cortex (15), andprime mover muscles begin to contract. The current obser-vations suggest a negative correlation between wrist-relatedmuscle or unit activity and LFP oscillations. However, in thedigit task, LFP oscillations often continued into the earlyphases of task performance, a time when both muscles andunits would be intensely active (17). Voluntary muscle acti-vation did not by itself completely suppress LFP oscillationsbecause oscillations often reappeared soon after the monkeyachieved a static torque required for liquid reinforcement.Thus, LFP oscillations in motor cortex seem not simplyrelated to active movement but to the myriad of processesleading up to generation of phasic muscle activity. They maybe related to neurons, termed "set" cells (18), with dischargepatterns that modulate during movement preparation (19-21). That oscillations occurred during the initial phases of thedigit task and occurred more frequently when monkeysperformed tasks requiring skilled digit or wrist manipulation(9) argues against a simple conclusion that only attentional

PMAA Thumb (w7)

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4474 Neurobiology: Sanes and Donoghue

states drive LFP oscillations. However, the complex rela-tionships between muscle, unit, and LFP activity suggest thatLFP oscillations are related to membrane potential fluctua-tions of only a subset of neurons or perhaps even corticalafferents.The data recorded in these experiments confirm that syn-

chronous activity between 15 and 50 Hz occurs in primaryand nonprimary motor cortical areas. Thus, oscilationsappear to be a general and prominent feature of motor, inaddition to sensory, cortex in alert animals, although onerecent report argues against a prominent role for neuraloscillations in information processing (22). Although thefrequencies ofLFP oscillations obtained in our two macaquemonkeys fell within described ranges (2, 3, 9), the dominantLFP oscillation frequency in the two animals diverged by>10 Hz. These differences were evident, even though themonkeys performed under nearly identical stimulus-re-sponse conditions. The differences in oscillation frequencymay be related to disparities in motor behavior of the twomonkeys. Indeed, there was greater stereotypy in the move-ments performed by monkey FD than those of monkey FC.We commonly observed robust correlations between

paired LFP recordings obtained within and between frontalmotor cortical fields. In MI, nearby (<2 mm) and far apart(>5 mm) sites exhibited comparable cross-correlograms,indicating not only did common neural processing occurthroughout MI and into PMA but that, contrary to priorobservations (9, 23), the strength of interaction did notdiminish with intracortical distance within or between cy-toarchitectonic fields. Finally, significant interactions oc-curred between paired LFP recordings in primary and nonpri-mary motor cortex, and they could be stronger than nearbyinteractions within the same field. Further investigations ofneural activity interactions occurring at paired sites withinand between defmed cortical areas may provide functionalcorrelates ofthe known connectivity patterns ofmotor cortex(24-26).Our data on intraareal correlations in frontal motor cortex

agree with reports of correlated activity between visualcortex areas. Synchrony ofLFP oscillations occurs betweenstriate and extrastriate visual cortex (12), and, from ourobservations, also between primary and nonprimary frontalmotor areas. Between visual cortical areas, Engel et al. (12)showed that sites with similar receptive field mapping instriate and extrastriate cortex exhibited stronger commonoscillatory responses than sites with unrelated receptivefields. In motor cortex, common oscillations occurred be-tween paired sites with similar and different representationsof motor actions, as revealed by intracortical electrical stim-ulation. Because MI sites representing different joints havecomplex interconnections (26), similarity of electrical stim-ulation effects might not be a predictor of intersite LFPcorrelation in MI and PMA. Instead, more complex behav-ioral properties of motor cortex neurons and a better under-standing of motor cortex organization may be more salientthan electrical stimulation effects in predicting intersite cor-relation magnitude.These studies leave unresolved the nature and source of

neural oscillations. Earlier studies suggested that oscillationsare correlated with common population neural activity (12).No such simple relationship like this seems to exist in motorcortex, though LFP oscillations occur more frequently during

movement preparation and less so at movement onset whenneural activity is high. Nevertheless, LFP oscillations couldreflect activity of those motor cortex cells related to move-ment preparatory or attentive states. The finding that fewerthan half the single- or multiple-unit neural recordings invisual cortex have periodic activity (27) reinforces the ideathat oscillations may reflect resonance among a select neuralsample. This speculation remains to be resolved.

We thank Dr. Gyongyi GaAl, Beth Hottenstein, Martin Nietham-mer, Dr. Selim Suner, and Dr. Jing Wang for assistance during theseexperiments. This work was supported by grants from the WhitehallFoundation, the Charles E. Culpeper Foundation, and the NationalInstitutes of Health (NS-25074).

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