Article

Cortical activity in the null space: permitting preparation without movement

  • Nature Neuroscience volume 17, pages 440448 (2014)
  • doi:10.1038/nn.3643
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Abstract

Neural circuits must perform computations and then selectively output the results to other circuits. Yet synapses do not change radically at millisecond timescales. A key question then is: how is communication between neural circuits controlled? In motor control, brain areas directly involved in driving movement are active well before movement begins. Muscle activity is some readout of neural activity, yet it remains largely unchanged during preparation. Here we find that during preparation, while the monkey holds still, changes in motor cortical activity cancel out at the level of these population readouts. Motor cortex can thereby prepare the movement without prematurely causing it. Further, we found evidence that this mechanism also operates in dorsal premotor cortex, largely accounting for how preparatory activity is attenuated in primary motor cortex. Selective use of 'output-null' vs. 'output-potent' patterns of activity may thus help control communication to the muscles and between these brain areas.

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References

  1. 1.

    & Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62, 171–189 (2009).

  2. 2.

    , & Free choice activates a decision circuit between frontal and parietal cortex. Nature 453, 406–409 (2008).

  3. 3.

    , & Decisions in changing conditions: the urgency-gating model. J. Neurosci. 29, 11560–11571 (2009).

  4. 4.

    Evidence for time-variant decision making. Eur. J. Neurosci. 24, 3628–3641 (2006).

  5. 5.

    & Learning to move machines with the mind. Trends Neurosci. 34, 61–75 (2011).

  6. 6.

    New insights into motor cortex. Neuron 71, 387–388 (2011).

  7. 7.

    & 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 (1989).

  8. 8.

    & Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J. Neurophysiol. 39, 1062–1068 (1976).

  9. 9.

    & The premotor cortex of the monkey. J. Neurosci. 2, 1329–1345 (1982).

  10. 10.

    , & Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. J. Neurophysiol. 96, 3130–3146 (2006).

  11. 11.

    , , & The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements. Behav. Brain Res. 18, 143–157 (1985).

  12. 12.

    & Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys. Exp. Brain Res. 83, 285–302 (1991).

  13. 13.

    & Covariation of primate dorsal premotor cell activity with direction and amplitude during a memorized-delay reaching task. J. Neurophysiol. 84, 152–165 (2000).

  14. 14.

    , , , & Neural variability in premotor cortex provides a signature of motor preparation. J. Neurosci. 26, 3697–3712 (2006).

  15. 15.

    & The predictive value for performance speed of preparatory changes in neuronal activity of the monkey motor and premotor cortex. Behav. Brain Res. 53, 35–49 (1993).

  16. 16.

    , & A central source of movement variability. Neuron 52, 1085–1096 (2006).

  17. 17.

    & Delay of movement caused by disruption of cortical preparatory activity. J. Neurophysiol. 97, 348–359 (2007).

  18. 18.

    , , , & Roles of primate spinal interneurons in preparation and execution of voluntary hand movement. Brain Res. Brain Res. Rev. 40, 53–65 (2002).

  19. 19.

    & Primate spinal interneurons show pre-movement instructed delay activity. Nature 401, 590–594 (1999).

  20. 20.

    , & Movement-related activity in the premotor cortex of rhesus macaques. Prog. Brain Res. 64, 117–131 (1986).

  21. 21.

    & Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Q. J. Exp. Physiol. 11, 135–222 (1917).

  22. 22.

    & Motor areas in the frontal lobe of the primate. Physiol. Behav. 77, 677–682 (2002).

  23. 23.

    , & Direct cortical control of 3D neuroprosthetic devices. Science 296, 1829–1832 (2002).

  24. 24.

    & Role of corticospinal suppression during motor preparation. Cereb. Cortex 19, 2013–2024 (2009).

  25. 25.

    , , , & Cortical preparatory activity: representation of movement or first cog in a dynamical machine? Neuron 68, 387–400 (2010).

  26. 26.

    & Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. J. Neurophysiol. 84, 986–1005 (2000).

  27. 27.

    , , & Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons. J. Neurophysiol. 81, 875–894 (1999).

  28. 28.

    et al. Roles of monkey premotor neuron classes in movement preparation and execution. J. Neurophysiol. 104, 799–810 (2010).

  29. 29.

    & Neural dynamics of planned arm movements: emergent invariants and speed-accuracy properties during trajectory formation. Psychol. Rev. 95, 49–90 (1988).

  30. 30.

    Integrated neural processes for defining potential actions and deciding between them: a computational model. J. Neurosci. 26, 9761–9770 (2006).

  31. 31.

    , & What roles do tonic inhibition and disinhibition play in the control of motor programs? Front. Behav. Neurosci. 4, 30 (2010).

  32. 32.

    , & Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. J. Neurophysiol. 47, 827–844 (1982).

  33. 33.

    , & The roles of monkey M1 neuron classes in movement preparation and execution. J. Neurophysiol. 110, 817–825 (2013).

  34. 34.

    , , & Low-dimensional neural features predict muscle EMG signals. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2010, 6027–6033 (2010).

  35. 35.

    , , & A dynamical systems view of motor preparation: implications for neural prosthetic system design. Prog. Brain Res. 192, 33–58 (2011).

  36. 36.

    & Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226–1235 (2002).

  37. 37.

    , & Cortical control of arm movements: a dynamical systems perspective. Annu. Rev. Neurosci. 36, 337–359 (2013).

  38. 38.

    et al. Neural population dynamics during reaching. Nature 487, 51–56 (2012).

  39. 39.

    & The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11, 667–689 (1991).

  40. 40.

    et al. Gaussian-process factor analysis for low-dimensional single-trial analysis of neural population activity. J. Neurophysiol. 102, 614–635 (2009).

  41. 41.

    et al. Heterogenous population coding of a short-term memory and decision task. J. Neurosci. 30, 916–929 (2010).

  42. 42.

    , & Functional, but not anatomical, separation of “what” and “when” in prefrontal cortex. J. Neurosci. 30, 350–360 (2010).

  43. 43.

    , , & Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 503, 78–84 (2013).

  44. 44.

    & Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J. Neurophysiol. 97, 4235–4257 (2007).

  45. 45.

    & Functional classes of primate corticomotoneuronal cells and their relation to active force. J. Neurophysiol. 44, 773–791 (1980).

  46. 46.

    & Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. J. Neurophysiol. 89, 2279–2288 (2003).

  47. 47.

    & Partial reconstruction of muscle activity from a pruned network of diverse motor cortex neurons. J. Neurophysiol. 97, 70–82 (2007).

  48. 48.

    , & Control of muscle synergies by cortical ensembles. Adv. Exp. Med. Biol. 629, 179–199 (2009).

  49. 49.

    , & Neural dynamics of reaching following incorrect or absent motor preparation. Neuron 81, 438–451 (2014).

  50. 50.

    et al. Single-trial neural correlates of arm movement preparation. Neuron 71, 555–564 (2011).

  51. 51.

    , & The construction of movement by the spinal cord. Nat. Neurosci. 2, 162–167 (1999).

  52. 52.

    , , & Techniques for extracting single-trial activity patterns from large-scale neural recordings. Curr. Opin. Neurobiol. 17, 609–618 (2007).

  53. 53.

    , & Neuronal population coding of movement direction. Science 233, 1416–1419 (1986).

  54. 54.

    , & Muscle and movement representations in the primary motor cortex. Science 285, 2136–2139 (1999).

  55. 55.

    & Motor cortical representation of speed and direction during reaching. J. Neurophysiol. 82, 2676–2692 (1999).

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Acknowledgements

We thank M. Mazariegos for expert surgical assistance and veterinary care, D. Haven for technical support and S. Eisensee for administrative support. This work was supported by a US National Science Foundation graduate research fellowship (M.T.K.), Burroughs Wellcome Fund Career Awards in the Biomedical Sciences (M.M.C., K.V.S.), the Christopher and Dana Reeve Foundation (S.I.R., K.V.S.), US National Institutes of Health (NIH) CRCNS R01-NS054283 (K.V.S.), NIH Director's Pioneer Award 1DP1OD006409 (K.V.S.) and US Defense Advanced Research Projects Agency REPAIR N66001-10-C-2010 (K.V.S.).

Author information

Affiliations

  1. Neurosciences Program, Stanford University, Stanford, California, USA.

    • Matthew T Kaufman
    •  & Krishna V Shenoy
  2. Department of Electrical Engineering, Stanford University, Stanford, California, USA.

    • Matthew T Kaufman
    • , Stephen I Ryu
    •  & Krishna V Shenoy
  3. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

    • Matthew T Kaufman
  4. Department of Neuroscience, Columbia University Medical Center, New York, New York, USA.

    • Mark M Churchland
  5. Grossman Center for the Statistics of Mind, Columbia University Medical Center, New York, New York, USA.

    • Mark M Churchland
  6. David Mahoney Center for Brain and Behavior Research, Columbia University Medical Center, New York, New York, USA.

    • Mark M Churchland
  7. Kavli Institute for Brain Science, Columbia University Medical Center, New York, New York, USA.

    • Mark M Churchland
  8. Department of Neurosurgery, Palo Alto Medical Foundation, Palo Alto, California, USA.

    • Stephen I Ryu
  9. Department of Bioengineering, Stanford University, Stanford, California, USA.

    • Krishna V Shenoy
  10. Department of Neurobiology, Stanford University, Stanford, California, USA.

    • Krishna V Shenoy

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Contributions

M.T.K. and M.M.C. designed and performed experiments. M.T.K. performed analyses and wrote the manuscript. S.I.R. performed array implantation surgery. K.V.S. oversaw all parts of experiments and writing.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Krishna V Shenoy.

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