Skip to main content
SpringerLink
Log in

Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We investigated how neurons in the different motor areas of the frontal lobe reflect the movement dynamics, and how their neuronal activity undergoes plastic changes when monkeys adapt to perturbing forces (they learn new dynamics). Here we describe the results obtained in the dorsal premotor area (PMd) and ventral premotor area (PMv). Monkeys performed visually instructed, delayed reaching movements before, during and after exposure and adaptation to a viscous, curl force field. During movement planning (i.e., during an instructed delay that followed the cue and preceded the go signal), we found dynamics-related activity in PMd but not in PMv. A closer analysis revealed that the population of PMd reflected the dynamics of the upcoming movement increasingly over the course of the delay, starting from a kinematics-related signal. During movement execution, dynamics-related activity was present in both PMd and PMv. In this respect, the results for PMd were similar to that previously found for the supplementary motor area (SMA) whereas the results for PMv were more similar to that previously found for the primary motor cortex (M1). Plastic changes associated with the acquisition of new dynamics found in PMd and PMv were qualitatively similar to those previously observed in M1 and SMA. The ensemble of our experiments suggest a broader picture of the cortical control of movements, whereby multiple areas all contribute to the various sensorimotor processes, including “low” computations such as the movement dynamics, but also express a degree of specialization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alexander GE, Crutcher MD (1990) Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J Neurophysiol 64:133–150

    PubMed  CAS  Google Scholar 

  • Boudreau MJ, Brochier T, Pare M, Smith AM (2001) Activity in ventral and dorsal premotor cortex in response to predictable force-pulse perturbations in a precision grip task. J Neurophysiol 86:1067–1078

    PubMed  CAS  Google Scholar 

  • Crammond DJ, Kalaska JF (1994) Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. J Neurophysiol 71:1281–1284

    PubMed  CAS  Google Scholar 

  • Crammond DJ, Kalaska JF (1996) Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task. Exp Brain Res 108:45–61

    Article  PubMed  CAS  Google Scholar 

  • Crutcher MD, Alexander GE (1990) Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey. J Neurophysiol 64:151–163

    PubMed  CAS  Google Scholar 

  • Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31:14–27

    PubMed  CAS  Google Scholar 

  • Fisher NI (1993) Statistical analysis of circular data. Cambridge University Press, Cambridge

    Google Scholar 

  • Fromm C (1983) Changes of steady state activity in motor cortex consistent with the length-tension relation of muscle. Pflugers Arch 398:318–323

    Article  PubMed  CAS  Google Scholar 

  • Gandolfo F, Li C, Benda BJ, Padoa-Schioppa C, Bizzi E (2000) Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97:2259–2263

    Article  PubMed  CAS  Google Scholar 

  • Graziano MS (1999) Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. Proc Natl Acad Sci USA 96:10418–10421

    Article  PubMed  CAS  Google Scholar 

  • Graziano MS, Hu XT, Gross CG (1997) Visuospatial properties of ventral premotor cortex. J Neurophysiol 77:2268–2292

    PubMed  CAS  Google Scholar 

  • He SQ, Dum RP, Strick PL (1993) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 13:952–980

    PubMed  CAS  Google Scholar 

  • He SQ, Dum RP, Strick PL (1995) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci 15:3284–3306

    PubMed  CAS  Google Scholar 

  • Hepp-Reymond MC, Husler EJ, Maier MA, Ql HX (1994) Force-related neuronal activity in two regions of the primate ventral premotor cortex. Can J Physiol Pharmacol 72:571–579

    PubMed  CAS  Google Scholar 

  • Hepp-Reymond M, Kirkpatrick-Tanner M, Gabernet L, Qi HX, Weber B (1999) Context-dependent force coding in motor and premotor cortical areas. Exp Brain Res 128:123–133

    Article  PubMed  CAS  Google Scholar 

  • Hoshi E, Tanji J (2002) Contrasting neuronal activity in the dorsal and ventral premotor areas during preparation to reach. J Neurophysiol 87:1123–1128

    PubMed  Google Scholar 

  • Johnson PB, Ferraina S, Bianchi L, Caminiti R (1996) Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6:102–119

    Article  PubMed  CAS  Google Scholar 

  • Johnson MT, Coltz JD, Hagen MC, Ebner TJ (1999) Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons. J Neurophysiol 81:875–894

    PubMed  CAS  Google Scholar 

  • Kakei S, Hoffman DS, Strick PL (2001) Direction of action is represented in the ventral premotor cortex. Nat Neurosci 4:1020–1025

    Article  PubMed  CAS  Google Scholar 

  • Kalaska JF, Cohen DA, Hyde ML, Prud’homme M (1989) A comparison of movement direction-related versus load direction-related activity in primate motor cortex, using a two-dimensional reaching task. J Neurosci 9:2080–2102

    PubMed  CAS  Google Scholar 

  • Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727

    Article  PubMed  CAS  Google Scholar 

  • Kurata K, Wise SP (1988) Premotor cortex of rhesus monkeys: set-related activity during two conditional motor tasks. Exp Brain Res 69:327–343

    Article  PubMed  CAS  Google Scholar 

  • Li CS, Padoa-Schioppa C, Bizzi E (2001) Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30:593–607

    Article  PubMed  CAS  Google Scholar 

  • Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140

    Article  PubMed  CAS  Google Scholar 

  • Luppino G, Matelli M, Camarda R, Rizzolatti G (1994) Corticospinal projections from mesial frontal and cingulate areas in the monkey. Neuroreport 5:2545–2548

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res 18:125–136

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445–462

    Article  PubMed  CAS  Google Scholar 

  • Mauritz KH, Wise SP (1986) Premotor cortex of the rhesus monkey: neuronal activity in anticipation of predictable environmental events. Exp Brain Res 61:229–244

    Article  PubMed  CAS  Google Scholar 

  • Mussa-Ivaldi FA, Bizzi E (2000) Motor learning through the combination of primitives. Philos Trans R Soc Lond B Biol Sci 355:1755–1769

    Article  PubMed  CAS  Google Scholar 

  • Padoa-Schioppa C, Li CS, Bizzi E (2002) Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron 36:751–765

    Article  PubMed  CAS  Google Scholar 

  • Padoa-Schioppa C, Li CS, Bizzi E (2004) Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. J Neurophysiol 91:449–473

    Article  PubMed  Google Scholar 

  • Riehle A, Requin J (1989) Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. J Neurophysiol 61:534–549

    PubMed  CAS  Google Scholar 

  • Rouiller EM, Moret V, Tanne J, Boussaoud D (1996) Evidence for direct connections between the hand region of the supplementary motor area and cervical motoneurons in the macaque monkey. Eur J Neurosci 8:1055–1059

    Article  PubMed  CAS  Google Scholar 

  • Saltzman E (1979) Levels of sensorimotor representation. J Math Psychol 20:91–163

    Article  Google Scholar 

  • Scott SH, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. J Neurophysiol 77:826–852

    PubMed  CAS  Google Scholar 

  • Scott SH, Sergio LE, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. J Neurophysiol 78:2413–2426

    PubMed  CAS  Google Scholar 

  • Shadmehr R, Moussavi ZM (2000) Spatial generalization from learning dynamics of reaching movements. J Neurosci 20:7807–7815

    PubMed  CAS  Google Scholar 

  • Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224

    PubMed  CAS  Google Scholar 

  • Shen L, Alexander GE (1997a) Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. J Neurophysiol 77:1171–1194

    CAS  Google Scholar 

  • Shen L, Alexander GE (1997b) Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. J Neurophysiol 77:1195–1212

    CAS  Google Scholar 

  • Thach WT (1978) Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. J Neurophysiol 41:654–676

    PubMed  CAS  Google Scholar 

  • Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19:8573–8588

    PubMed  CAS  Google Scholar 

  • Werner W, Bauswein E, Fromm C (1991) Static firing rates of premotor and primary motor cortical neurons associated with torque and joint position. Exp Brain Res 86:293–302

    Article  PubMed  CAS  Google Scholar 

  • Wise SP, Mauritz KH (1985) Set-related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set. Proc R Soc Lond B Biol Sci 223:331–354

    Article  PubMed  CAS  Google Scholar 

  • Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3(Suppl):1212–1217

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Institute of Health (NIH grant MN481185).

Author information

Authors and Affiliations

  1. McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA

    Jun Xiao, Camillo Padoa-Schioppa & Emilio Bizzi

  2. Department of Biology, City College of New York, New York, USA

    Jun Xiao

  3. Department of Neurobiology, Harvard Medical School, Boston, MA, 02115, USA

    Camillo Padoa-Schioppa

Authors
  1. Jun Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camillo Padoa-Schioppa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emilio Bizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emilio Bizzi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xiao, J., Padoa-Schioppa, C. & Bizzi, E. Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey. Exp Brain Res 168, 106–119 (2006). https://doi.org/10.1007/s00221-005-0074-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0074-2

Keywords

Search

Navigation