Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonism

Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonism Many studies suggest that Parkinson’s disease (PD) is associated with changes in neuronal activity patterns throughout the basal ganglia-thalamocortical motor circuit. There are limited electrophysiological data, however, describing how parkinsonism impacts the presupplementary motor area (pre-SMA) and SMA proper (SMAp), cortical areas known to be involved in movement planning and motor control. In this study, local field potentials (LFPs) were recorded in the pre-SMA/SMAp of a nonhuman primate during a visually cued reaching task. Recordings were made in the same subject in both the naive and parkinsonian state using the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of parkinsonism. We found that in the naive animal, well before a go-cue providing instruction of reach onset and direction was given, LFP activity was dynamically modulated in both high (20–30 Hz) and low beta (10–20 Hz) bands, and the magnitude of this modulation (e.g., decrease/increase in beta amplitude for each band, respectively) correlated linearly with reaction time (RT) on a trial-to-trial basis, suggesting it may predictively encode for RT. Consistent with this hypothesis, we observed that this activity was more prominent within the pre-SMA compared with SMAp. In the parkinsonian state, however, pre-SMA/SMAp beta band modulation was disrupted, particularly in the high beta band, such that the predictive encoding of RT was significantly diminished. In addition, the predictive encoding of RT preferentially within pre-SMA over SMAp was lost. These findings add to our understanding of the role of pre-SMA/SMAp in motor behavior and suggest a fundamental role of these cortical areas in early preparatory and premovement processes that are altered in parkinsonism. NEW & NOTEWORTHY Goal-directed movements, such as reaching for an object, necessitate temporal preparation and organization of information processing within the basal ganglia-thalamocortical motor network. Impaired movement in parkinsonism is thought to be the result of pathophysiological activity disrupting information flow within this network. This work provides neurophysiological evidence linking altered motor preplanning processes encoded in pre-SMA/SMAp beta band modulation to the pathogenesis of motor disturbances in parkinsonism. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Neurophysiology The American Physiological Society

Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonism

9 pages
Read Article

Loading next page...
 
/lp/aps/predictive-encoding-of-motor-behavior-in-the-supplementary-motor-area-hAfYRlERdZ
ISSN
0022-3077
eISSN
1522-1598
D.O.I.
10.1152/jn.00306.2018
Publisher site
See Article on Publisher Site

Abstract

Many studies suggest that Parkinson’s disease (PD) is associated with changes in neuronal activity patterns throughout the basal ganglia-thalamocortical motor circuit. There are limited electrophysiological data, however, describing how parkinsonism impacts the presupplementary motor area (pre-SMA) and SMA proper (SMAp), cortical areas known to be involved in movement planning and motor control. In this study, local field potentials (LFPs) were recorded in the pre-SMA/SMAp of a nonhuman primate during a visually cued reaching task. Recordings were made in the same subject in both the naive and parkinsonian state using the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of parkinsonism. We found that in the naive animal, well before a go-cue providing instruction of reach onset and direction was given, LFP activity was dynamically modulated in both high (20–30 Hz) and low beta (10–20 Hz) bands, and the magnitude of this modulation (e.g., decrease/increase in beta amplitude for each band, respectively) correlated linearly with reaction time (RT) on a trial-to-trial basis, suggesting it may predictively encode for RT. Consistent with this hypothesis, we observed that this activity was more prominent within the pre-SMA compared with SMAp. In the parkinsonian state, however, pre-SMA/SMAp beta band modulation was disrupted, particularly in the high beta band, such that the predictive encoding of RT was significantly diminished. In addition, the predictive encoding of RT preferentially within pre-SMA over SMAp was lost. These findings add to our understanding of the role of pre-SMA/SMAp in motor behavior and suggest a fundamental role of these cortical areas in early preparatory and premovement processes that are altered in parkinsonism. NEW & NOTEWORTHY Goal-directed movements, such as reaching for an object, necessitate temporal preparation and organization of information processing within the basal ganglia-thalamocortical motor network. Impaired movement in parkinsonism is thought to be the result of pathophysiological activity disrupting information flow within this network. This work provides neurophysiological evidence linking altered motor preplanning processes encoded in pre-SMA/SMAp beta band modulation to the pathogenesis of motor disturbances in parkinsonism.

Journal

Journal of Neurophysiology – The American Physiological Society

Published: Sep 1, 2018

References

  • Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output
    Akkal, D; Dum, RP; Strick, PL
  • The functional anatomy of basal ganglia disorders
    Albin, RL; Young, AB; Penney, JB
  • Functional architecture of basal ganglia circuits: neural substrates of parallel processing
    Alexander, GE; Crutcher, MD
  • The scalable brain atlas: instant web-based access to public brain atlases and related content
    Bakker, R; Tiesinga, P; Kötter, R
  • Perceptual factors contribute to akinesia in Parkinson’s disease
    Ballanger, B; Gil, R; Audiffren, M; Desmurget, M
  • Changes in resting-state directed connectivity in cortico-subcortical networks correlate with cognitive function in Parkinson’s disease
    Boon, LI; Hillebrand, A; Olde Dubbelink, KTE; Stam, CJ; Berendse, HW
  • Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson’s disease
    Brown, P
  • What do the basal ganglia do?
    Brown, P; Marsden, CD
  • Influential observations, high leverage points, and outliers in linear regression
    Chatterjee, S; Hadi, AS
  • Sources of bias in single-trial normalization procedures
    Ciuparu, A; Mureşan, RC
  • Modulations in oscillatory frequency and coupling in globus pallidus with increasing parkinsonian severity
    Connolly, AT; Jensen, AL; Bello, EM; Netoff, TI; Baker, KB; Johnson, MD; Vitek, JL
  • Local field potential recordings in a non-human primate model of Parkinsons disease using the Activa PC + S neurostimulator
    Connolly, AT; Muralidharan, A; Hendrix, C; Johnson, L; Gupta, R; Stanslaski, S; Denison, T; Baker, KB; Vitek, JL; Johnson, MD
  • Dynamics of executive control and motor deficits in parkinsonian rats
    Courtière, A; Hardouin, J; Burle, B; Vidal, F; Turle-Lorenzo, N; Amalric, M; Hasbroucq, T
  • Selective effects of low-dose dopamine D1 and D2 receptor antagonists on rat information processing
    Courtière, A; Hardouin, J; Goujon, A; Vidal, F; Hasbroucq, T
  • Motor imagery in Parkinson’s disease: a PET study
    Cunnington, R; Egan, GF; O’Sullivan, JD; Hughes, AJ; Bradshaw, JL; Colebatch, JG
  • The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response
    Cunnington, R; Windischberger, C; Deecke, L; Moser, E
  • Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring
    Debener, S; Ullsperger, M; Siegel, M; Fiehler, K; von Cramon, DY; Engel, AK
  • Lateralization of event-related beta desynchronization in the EEG during pre-cued reaction time tasks
    Doyle, LMF; Yarrow, K; Brown, P
  • BrainInfo online 3D macaque brain atlas: a database in the shape of a brain
    Dubach, MF; Bowden, DM
  • A method for quantitating motor deficits in a nonhuman primate following MPTP-induced hemiparkinsonism and co-grafting
    Ellis, JE; Byrd, LD; Bakay, RAE
  • Beta-band oscillations—signalling the status quo?
    Engel, AK; Fries, P
  • Invasive recordings from the human brain: clinical insights and beyond
    Engel, AK; Moll, CKE; Fried, I; Ojemann, GA
  • Parkinsonism and vigilance: alteration in neural oscillatory activity and phase-amplitude coupling in the basal ganglia and motor cortex
    Escobar Sanabria, D; Johnson, LA; Nebeck, SD; Zhang, J; Johnson, MD; Baker, KB; Molnar, GF; Vitek, JL
  • Disruption of information processing in the supplementary motor area of the MPTP-treated monkey: a clue to the pathophysiology of akinesia?
    Escola, L; Michelet, T; Macia, F; Guehl, D; Bioulac, B; Burbaud, P
  • Networks mediating the clinical effects of pallidal brain stimulation for Parkinson’s disease: a PET study of resting-state glucose metabolism
    Fukuda, M; Mentis, MJ; Ma, Y; Dhawan, V; Antonini, A; Lang, AE; Lozano, AM; Hammerstad, J; Lyons, K; Koller, WC; Moeller, JR; Eidelberg, D
  • Pathophysiology of parkinsonism
    Galvan, A; Wichmann, T
  • Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system
    Gilbertson, T; Lalo, E; Doyle, L; Di Lazzaro, V; Cioni, B; Brown, P
  • Single-trial normalization for event-related spectral decomposition reduces sensitivity to noisy trials
    Grandchamp, R; Delorme, A
  • Prestimulus oscillations predict visual perception performance between and within subjects
    Hanslmayr, S; Aslan, A; Staudigl, T; Klimesch, W; Herrmann, CS; Bäuml, K-H
  • Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa
    Haslinger, B; Erhard, P; Kämpfe, N; Boecker, H; Rummeny, E; Schwaiger, M; Conrad, B; Ceballos-Baumann, AO
  • Cue-related temporal factors modulate movement-related beta oscillatory activity in the human motor circuit
    Heinrichs-Graham, E; Arpin, DJ; Wilson, TW
  • Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging
    Heinrichs-Graham, E; Wilson, TW
  • Modulations in pallidal local field potentials in the systemic 1-methyl-4-phenyl-l, 2, 3, 6-tetrahydropyridine nonhuman primate model of Parkinson’s disease during a voluntary reaching task
    Hendrix, C; Agnesi, F; Connolly, AT; Baker, KB; Johnson, MD; Vitek, JL
  • EEG oscillations and wavelet analysis
    Herrmann, CS; Grigutsch, M; Busch, NA; Handy, TC
  • Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms
    Hikosaka, O; Isoda, M
  • Arm-use dependent lateralization of gamma and beta oscillations in primate medial motor areas
    Hosaka, R; Nakajima, T; Aihara, K; Yamaguchi, Y; Mushiake, H
  • The suppression of beta oscillations in the primate supplementary motor complex reflects a volatile state during the updating of action sequences
    Hosaka, R; Nakajima, T; Aihara, K; Yamaguchi, Y; Mushiake, H
  • Cognitive motor control in human pre-supplementary motor area studied by subdural recording of discrimination/selection-related potentials
    Ikeda, A; Yazawa, S; Kunieda, T; Ohara, S; Terada, K; Mikuni, N; Nagamine, T; Taki, W; Kimura, J; Shibasaki, H
  • The ups and downs of β oscillations in sensorimotor cortex
    Kilavik, BE; Zaepffel, M; Brovelli, A; MacKay, WA; Riehle, A
  • Digital bispectral analysis and its applications to nonlinear wave interactions
    Kim, YC; Powers, EJ
  • Network effects and pathways in deep brain stimulation in Parkinson’s disease
    Koirala, N; Fleischer, V; Granert, O; Deuschl, G; Muthuraman, M; Groppa, S
  • Disrupted nodal and hub organization account for brain network abnormalities in Parkinson’s disease
    Koshimori, Y; Cho, S-S; Criaud, M; Christopher, L; Jacobs, M; Ghadery, C; Coakeley, S; Harris, M; Mizrahi, R; Hamani, C; Lang, AE; Houle, S; Strafella, AP
  • Decreased parvalbumin mRNA expression in dorsolateral prefrontal cortex in Parkinson’s disease
    Lanoue, AC; Blatt, GJ; Soghomonian, J-J
  • Attention to intention
    Lau, HC; Rogers, RD; Haggard, P; Passingham, RE
  • Neural correlates of advance movement preparation: a dipole source analysis approach
    Leuthold, H; Jentzsch, I
  • Prestimulus oscillations enhance psychophysical performance in humans
    Linkenkaer-Hansen, K; Nikulin, VV; Palva, S; Ilmoniemi, RJ; Palva, JM
  • The functional role of beta oscillations in Parkinson’s disease
    Little, S; Brown, P
  • Common atlas format and 3D brain atlas reconstructor: infrastructure for constructing 3D brain atlases
    Majka, P; Kublik, E; Furga, G; Wójcik, DK
  • Nonparametric statistical testing of EEG- and MEG-data
    Maris, E; Oostenveld, R
  • A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task
    Matsuzaka, Y; Aizawa, H; Tanji, J
  • Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex
    Matsuzaka, Y; Tanji, J
  • Stereotactic neurosurgical planning, recording, and visualization for deep brain stimulation in non-human primates
    Miocinovic, S; Zhang, J; Xu, W; Russo, GS; Vitek, JL; McIntyre, CC
  • The role of the pre-supplementary motor area in the control of action
    Nachev, P; Wydell, H; O’Neill, K; Husain, M; Kennard, C
  • Intended arm use influences interhemispheric correlation of β-oscillations in primate medial motor areas
    Nakajima, T; Arisawa, H; Hosaka, R; Mushiake, H
  • Functional significance of the cortico-subthalamo-pallidal hyperdirect pathway
    Nambu, A; Tokuno, H; Takada, M
  • Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates
    Neuper, C; Pfurtscheller, G
  • FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data
    Oostenveld, R; Fries, P; Maris, E; Schoffelen, J-M
  • Prefrontal D1 dopamine signaling is necessary for temporal expectation during reaction time performance
    Parker, KL; Alberico, SL; Miller, AD; Narayanan, NS
  • Dopamine neurons encode errors in predicting movement trigger occurrence
    Pasquereau, B; Turner, RS
  • Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement
    Pfurtscheller, G; Aranibar, A
  • Post-movement beta synchronization. A correlate of an idling motor area?
    Pfurtscheller, G; Stancák, A; Neuper, C
  • Imaging the premotor areas
    Picard, N; Strick, PL
  • The INIA19 template and NeuroMaps atlas for primate brain image parcellation and spatial normalization
    Rohlfing, T; Kroenke, CD; Sullivan, EV; Dubach, MF; Bowden, DM; Grant, KA; Pfefferbaum, A
  • Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study
    Sabatini, U; Boulanouar, K; Fabre, N; Martin, F; Carel, C; Colonnese, C; Bozzao, L; Berry, I; Montastruc, JL; Chollet, F; Rascol, O
  • Normal and pathological oscillatory communication in the brain
    Schnitzler, A; Gross, J
  • Functional dissociation of pre-SMA and SMA-proper in temporal processing
    Schwartze, M; Rothermich, K; Kotz, SA
  • Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study
    Senkowski, D; Molholm, S; Gomez-Ramirez, M; Foxe, JJ
  • Basic mechanisms of central rhythms reactivity to preparation and execution of a voluntary movement: a stereoelectroencephalographic study
    Szurhaj, W; Derambure, P; Labyt, E; Cassim, F; Bourriez, J-L; Isnard, J; Guieu, J-D; Mauguière, F
  • Motor imagery in normal subjects and in asymmetrical Parkinson’s disease: a PET study
    Thobois, S; Dominey, PF; Decety, J; Pollak, PP; Gregoire, MC; Le Bars, PD; Broussolle, E
  • The role of dopamine in temporal uncertainty
    Tomassini, A; Ruge, D; Galea, JM; Penny, W; Bestmann, S
  • How to evaluate phase differences between trial groups in ongoing electrophysiological signals
    VanRullen, R
  • External pallidal stimulation improves parkinsonian motor signs and modulates neuronal activity throughout the basal ganglia thalamic network
    Vitek, JL; Zhang, J; Hashimoto, T; Russo, GS; Baker, KB
  • Network-wide oscillations in the parkinsonian state: alterations in neuronal activities occur in the premotor cortex in parkinsonian nonhuman primates
    Wang, J; Johnson, LA; Jensen, AL; Baker, KB; Molnar, GF; Johnson, MD; Vitek, JL
  • Effects of rTMS of pre-supplementary motor area on fronto basal ganglia network activity during stop-signal task
    Watanabe, T; Hanajima, R; Shirota, Y; Tsutsumi, R; Shimizu, T; Hayashi, T; Terao, Y; Ugawa, Y; Katsura, M; Kunimatsu, A; Ohtomo, K; Hirose, S; Miyashita, Y; Konishi, S
  • Basal ganglia, movement disorders and deep brain stimulation: advances made through non-human primate research
    Wichmann, T; Bergman, H; DeLong, MR
  • Prestimulus cortical activity is correlated with speed of visuomotor processing
    Zhang, Y; Wang, X; Bressler, SL; Chen, Y; Ding, M

You’re reading a free preview. Subscribe to read the entire article.

Try 2 weeks free now

DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

or browse the journals available

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create folders to
organize your research

Export folders, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off

Sign up
for free
Start 14 day
Free Trial