M1 corticospinal mirror neurons and their role in movement suppression during action observation

Ganesh Vigneswaran, Roland Philipp, Roger N Lemon, Alexander Kraskov, Ganesh Vigneswaran, Roland Philipp, Roger N Lemon, Alexander Kraskov

Abstract

Evidence is accumulating that neurons in primary motor cortex (M1) respond during action observation, a property first shown for mirror neurons in monkey premotor cortex. We now show for the first time that the discharge of a major class of M1 output neuron, the pyramidal tract neuron (PTN), is modulated during observation of precision grip by a human experimenter. We recorded 132 PTNs in the hand area of two adult macaques, of which 65 (49%) showed mirror-like activity. Many (38 of 65) increased their discharge during observation (facilitation-type mirror neuron), but a substantial number (27 of 65) exhibited reduced discharge or stopped firing (suppression-type). Simultaneous recordings from arm, hand, and digit muscles confirmed the complete absence of detectable muscle activity during observation. We compared the discharge of the same population of neurons during active grasp by the monkeys. We found that facilitation neurons were only half as active for action observation as for action execution, and that suppression neurons reversed their activity pattern and were actually facilitated during execution. Thus, although many M1 output neurons are active during action observation, M1 direct input to spinal circuitry is either reduced or abolished and may not be sufficient to produce overt muscle activity.

Copyright © 2013 Elsevier Ltd. All rights reserved.

Figures

Figure 1
Figure 1
Experimental Apparatus (A and B) The diagram shows the monkey’s perspective of a carousel device used to present an object during execution (A) or observation trials (B). Notations: HP-M, homepads monkey, left (L) and right (R); HP-H, homepad experimenter; S-E and S-O, screens that could be electronically switched from opaque to transparent during execution (S-E) or observation trials (S-O), allowing the monkey a direct view of the object (OBJ-M) when the monkey grasped it (A) and of the same object (OBJ-H) when the experimenter grasped it (B). (C) Close-up of the trapezoid object (affords precision grip) mounted on a spring-loaded shuttle. (D) Side view of monkey grasping the trapezoid object using precision grip. (E–H) Average EMG traces from 11 hand or arm muscles from one session in monkey M47 for execution (E) and observation trials (F). During execution, all muscles were active, but there was no modulation during observation. Note that a ten times higher gain was used for observation trials to emphasize absence of EMG activity (note different y scale). Averages are aligned to the onset of the object displacement (DO) by the monkey (E) or human (F). Average displacement of the object is shown for execution and observation trials in (G) and (H), respectively. The median times of other recorded events relative to DO are shown as vertical lines above. Muscles are color-coded as shown in key at right of (F) and are abbreviated as follows: AbPl, abductor pollicis longus; deltoid; thenar; ECU, extensor carpi ulnaris; EDC, extensor digitorum communis; ECRL, extensor carpi radialis longus; FDP, flexor digitorum profundus; FCU, flexor carpi ulnaris; 1DI, first dorsal interosseous; Palm, palmaris; BRR, brachioradialis. Notations: GO, go cue; HPR, homepad release; HON, stable hold onset; HOFF, stable hold offset.
Figure 2
Figure 2
Mirror PTNs in M1 Examples of M1 facilitation (A and C) and suppression (B and D) mirror PTNs in M47 (A and B) and M43 (C and D). Each panel consists of raster plots for observation and execution trials and corresponding histograms (solid and dashed lines, respectively). Histograms were compiled in 20 ms bins and then smoothed using a 140 ms sliding window. In (A) and (B), all data were aligned to onset of the object displacement (DO); other behavioral events are indicated by colored markers for each trial on raster plots and with vertical lines on histograms (cf. Figure 1). In (C) and (D), all execution trial data were aligned to movement onset (MO), defined using onset of biceps EMG activity. All observation trial data were aligned to a sensor signal (S), which detected first contact of the experimenter with the object. HPR indicates beginning of the experimenter’s movement in observation trials. GO markers indicate the cue for the monkey to grasp the reward in execution trials.
Figure 3
Figure 3
Population Activity of M1 Mirror Neurons (A and B) Pie charts showing different types of facilitation (red, F) and suppression (blue, S) PTNs recorded during action observation (Obs in inset box) in M47 (A) and M43 (B). Lighter shades of both colors indicate proportions of these neurons whose discharge was facilitated during execution (Exec in inset box); darker shades indicate proportions showing suppression during execution (a relatively small proportion). ns, nonsignificant change in modulation during execution. (C) Left: population averages during observation for corticospinal mirror neurons (M47) that were activated during execution and whose discharge was significantly suppressed (blue) or facilitated (red) during observation (together with SEM, shaded areas). Firing rates were normalized to the absolute maximum of the smoothed averaged firing rate of individual neurons defined during execution and observation trials, and baseline firing rate was subtracted. Data aligned to DO, the median (black line), and the 25th to 75th percentile times of other events recorded are shown as shaded areas: GO (green), HPR (magenta), hold HON (cyan), and HOFF (yellow). Firing rates were smoothed using a 400 ms sliding window in 20 ms steps. Right: population average for the same groups of mirror neurons during execution. Facilitation-type PTNs showed higher discharge rates during execution compared with observation trials, and suppression type PTNs changed pattern to facilitation during execution. (D) Maximum firing rate of PTNs during observation and execution trials, expressed as raw firing rates (with SEM). Results from both monkeys were pooled. Red bars show average rates for 38 M1 PTNs facilitated during both observation (O) and execution (E) (F-F type). Note the much lower rate during observation. Blue bars show rates for 27 M1 PTNs suppressed during observation (O) and facilitated during execution (E) (S-F type). The left green bar shows the mean firing rate for all these mirror PTNs in observation minus that in execution, to capture the total amount of disfacilitation in the output from these neurons that occurred during observation. On the right are similar results for PTNs that did not show any mirror activity.

References

    1. Tkach D., Reimer J., Hatsopoulos N.G. Congruent activity during action and action observation in motor cortex. J. Neurosci. 2007;27:13241–13250.
    1. Dushanova J., Donoghue J. Neurons in primary motor cortex engaged during action observation. Eur. J. Neurosci. 2010;31:386–398.
    1. Gallese V., Fadiga L., Fogassi L., Rizzolatti G. Action recognition in the premotor cortex. Brain. 1996;119:593–609.
    1. Rizzolatti G., Fadiga L., Gallese V., Fogassi L. Premotor cortex and the recognition of motor actions. Brain Res. Cogn. Brain Res. 1996;3:131–141.
    1. Kakei S., Hoffman D.S., Strick P.L. Muscle and movement representations in the primary motor cortex. Science. 1999;285:2136–2139.
    1. Todorov E. Direct cortical control of muscle activation in voluntary arm movements: a model. Nat. Neurosci. 2000;3:391–398.
    1. Lemon R.N. Descending pathways in motor control. Annu. Rev. Neurosci. 2008;31:195–218.
    1. Scott S.H. Inconvenient truths about neural processing in primary motor cortex. J. Physiol. 2008;586:1217–1224.
    1. Fadiga L., Fogassi L., Pavesi G., Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 1995;73:2608–2611.
    1. Hari R., Forss N., Avikainen S., Kirveskari E., Salenius S., Rizzolatti G. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc. Natl. Acad. Sci. USA. 1998;95:15061–15065.
    1. Montagna M., Cerri G., Borroni P., Baldissera F. Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action. Eur. J. Neurosci. 2005;22:1513–1520.
    1. Press C., Cook J., Blakemore S.J., Kilner J. Dynamic modulation of human motor activity when observing actions. J. Neurosci. 2011;31:2792–2800.
    1. Szameitat A.J., Shen S., Conforto A., Sterr A. Cortical activation during executed, imagined, observed, and passive wrist movements in healthy volunteers and stroke patients. Neuroimage. 2012;62:266–280.
    1. Cisek P., Kalaska J.F. Neural correlates of mental rehearsal in dorsal premotor cortex. Nature. 2004;431:993–996.
    1. Dum R.P., Strick P.L. The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 1991;11:667–689.
    1. Porter R., Lemon R. Oxford University Press; Oxford: 1993. Corticospinal Function and Voluntary Movement (Monographs of the Physiological Society 45)
    1. Rizzolatti G., Luppino G. The cortical motor system. Neuron. 2001;31:889–901.
    1. Kraskov A., Dancause N., Quallo M.M., Shepherd S., Lemon R.N. Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression? Neuron. 2009;64:922–930.
    1. Maier M.A., Bennett K.M., Hepp-Reymond M.C., Lemon R.N. Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. J. Neurophysiol. 1993;69:772–785.
    1. Molenberghs P., Cunnington R., Mattingley J.B. Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci. Biobehav. Rev. 2012;36:341–349.
    1. Nelissen K., Borra E., Gerbella M., Rozzi S., Luppino G., Vanduffel W., Rizzolatti G., Orban G.A. Action observation circuits in the macaque monkey cortex. J. Neurosci. 2011;31:3743–3756.
    1. Nelissen K., Luppino G., Vanduffel W., Rizzolatti G., Orban G.A. Observing others: multiple action representation in the frontal lobe. Science. 2005;310:332–336.
    1. Borra E., Belmalih A., Gerbella M., Rozzi S., Luppino G. Projections of the hand field of the macaque ventral premotor area F5 to the brainstem and spinal cord. J. Comp. Neurol. 2010;518:2570–2591.
    1. He S.Q., Dum R.P., Strick P.L. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J. Neurosci. 1993;13:952–980.
    1. Stamos A.V., Savaki H.E., Raos V. The spinal substrate of the suppression of action during action observation. J. Neurosci. 2010;30:11605–11611.
    1. Olivier E., Baker S.N., Nakajima K., Brochier T., Lemon R.N. Investigation into non-monosynaptic corticospinal excitation of macaque upper limb single motor units. J. Neurophysiol. 2001;86:1573–1586.
    1. Jackson A., Baker S.N., Fetz E.E. Tests for presynaptic modulation of corticospinal terminals from peripheral afferents and pyramidal tract in the macaque. J. Physiol. 2006;573:107–120.
    1. Quallo M.M., Kraskov A., Lemon R.N. The activity of primary motor cortex corticospinal neurons during tool use by macaque monkeys. J. Neurosci. 2012;32:17351–17364.
    1. Fadiga L., Craighero L., Olivier E. Human motor cortex excitability during the perception of others’ action. Curr. Opin. Neurobiol. 2005;15:213–218.
    1. Jackson A., Spinks R.L., Freeman T.C.B., Wolpert D.M., Lemon R.N. Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation. J. Physiol. 2002;541:685–699.
    1. Weiler N., Wood L., Yu J., Solla S.A., Shepherd G.M. Top-down laminar organization of the excitatory network in motor cortex. Nat. Neurosci. 2008;11:360–366.
    1. Aron A.R., Durston S., Eagle D.M., Logan G.D., Stinear C.M., Stuphorn V. Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition. J. Neurosci. 2007;27:11860–11864.
    1. Duque J., Labruna L., Verset S., Olivier E., Ivry R.B. Dissociating the role of prefrontal and premotor cortices in controlling inhibitory mechanisms during motor preparation. J. Neurosci. 2012;32:806–816.
    1. Gilbertson T., Lalo E., Doyle L., Di Lazzaro V., Cioni B., Brown P. Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system. J. Neurosci. 2005;25:7771–7779.
    1. Carmena J.M., Lebedev M.A., Crist R.E., O’Doherty J.E., Santucci D.M., Dimitrov D.F., Patil P.G., Henriquez C.S., Nicolelis M.A. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol. 2003;1:E42.
    1. Davidson A.G., Chan V., O’Dell R., Schieber M.H. Rapid changes in throughput from single motor cortex neurons to muscle activity. Science. 2007;318:1934–1937.
    1. Fetz E.E., Cheney P.D. Functional relations between primate motor cortex cells and muscles: fixed and flexible. Ciba Found. Symp. 1987;132:98–117.
    1. Fetz E.E., Finocchio D.V. Operant conditioning of specific patterns of neural and muscular activity. Science. 1971;174:431–435.
    1. Schieber M.H. Dissociating motor cortex from the motor. J. Physiol. 2011;589:5613–5624.
    1. Vigneswaran G., Kraskov A., Lemon R.N. Large identified pyramidal cells in macaque motor and premotor cortex exhibit “thin spikes”: implications for cell type classification. J. Neurosci. 2011;31:14235–14242.
    1. Quiroga R.Q., Nadasdy Z., Ben-Shaul Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 2004;16:1661–1687.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться