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3 - A New View of the Motor Cortex and Its Relation to Social Behavior

from Part I - Foundations

Published online by Cambridge University Press:  27 October 2016

By
Michael S. A. Graziano
Edited by
Sukhvinder S. Obhi  and
Emily S. Cross
Sukhvinder S. Obhi
Affiliation:
McMaster University, Ontario
Emily S. Cross
Affiliation:
Bangor University
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Summary

Abstract

Three main views of the primate motor cortex have been proposed over the 140 years of its study. These views are not necessarily incompatible. In the homunculus view, the motor cortex functions as a rough map of the body’s musculature. In the population-code view, populations of broadly-tuned neurons combine to specify hand direction or some other parameter of movement. In the recently proposed action map view, common actions in the movement repertoire are emphasized in different regions of cortex. In the action map view, to fully understand the organization of the motor cortex, it is necessary to study the structure and complexity of the movement repertoire and understand how that statistical structure is mapped onto the cortical surface. This chapter discusses the action map in the primate brain and how some of the complex actions represented there may play a role in social behavior.

Type
Chapter
Information
Shared Representations
Sensorimotor Foundations of Social Life
 , pp. 38 - 58
Publisher: Cambridge University Press
Print publication year: 2016

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References

Aflalo, T. N., & Graziano, M. S. A. (2006a). Partial tuning of motor cortex neurons to final posture in a free-moving paradigm. Proceedings of the National Academy of Sciences, 103, 2909–2914.CrossRefGoogle Scholar
Aflalo, T. N., (2006b). Possible origins of the complex topographic organization of motor cortex: Reduction of a multidimensional space onto a two-dimensional array. Journal of Neuroscience, 26, 6288–6297.CrossRefGoogle ScholarPubMed
Aflalo, T. N., (2007). Relationship between unconstrained arm movement and single neuron firing in the macaque motor cortex. Journal of Neuroscience, 27, 2760–2780.CrossRefGoogle ScholarPubMed
Andrew, R. J. (1962). The origin and evolution of the calls and facial expressions of the primates. Behaviour, 20, 1–107.CrossRefGoogle Scholar
Asanuma, H. (1975). Recent developments in the study of the columnar arrangement of neurons within the motor cortex. Physiological Reviews, 55, 143–156.CrossRefGoogle Scholar
Bonazzi, L., Viaro, R., Lodi, E., Canto, R., Bonifazzi, C., & Franchi, G. (2013). Complex movement topography and extrinsic space representation in the rat forelimb motor cortex as defined by long-duration intracortical microstimulation. Journal of Neuroscience, 33, 2097–2107.CrossRefGoogle ScholarPubMed
Brozzoli, C., Gentile, G., Bergouignan, L., & Ehrsson, H. H. (2013). A shared representation of the space near oneself and others in the human premotor cortex. Current Biology, 23, 1764–1768.CrossRefGoogle ScholarPubMed
Bruce, C. J., Goldberg, M. E., Bushnell, M.C., & Stanton, G. B. (1985). Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. Journal of Neurophysiology, 54, 714–734.CrossRefGoogle ScholarPubMed
Caggiula, A. R., & Hoebel, B. G. (1966). ‘Copulation-reward site’ in the posterior hypothalamus. Science, 153, 1284–1285.CrossRefGoogle ScholarPubMed
Caruana, F., Jezzini, A., Sbriscia-Fioretti, B., Rizzolatti, G., & Gallese, V (2011). Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey. Current Biology, 21, 195–199.CrossRefGoogle ScholarPubMed
Chakrabarty, S., & Martin, J. H. (2000). Postnatal development of the motor representation in primary motor cortex. Journal of Neurophysiology, 84, 2582–2594.CrossRefGoogle ScholarPubMed
Cheney, P. D., & Fetz, E. E. (1985). Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: Evidence for functional groups of CM cells. Journal of Neurophysiology, 53, 786–804.CrossRefGoogle ScholarPubMed
Churchland, M. M., & Shenoy, K. V. (2007). Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. Journal of Neurophysiology, 97, 4235–4257.CrossRefGoogle ScholarPubMed
Cooke, D. F., & Graziano, M. S. A. (2003). Defensive movements evoked by air puff in monkeys. Journal of Neurophysiology, 90, 3317–3329.CrossRefGoogle ScholarPubMed
Cooke, D. F., (2004a). Sensorimotor integration in the precentral gyrus: Polysensory neurons and defensive movements. Journal of Neurophysiology, 91, 1648–1650.CrossRefGoogle ScholarPubMed
Cooke, D. F., (2004b). Super-flinchers and nerves of steel: Defensive movements altered by chemical manipulation of a cortical motor area. Neuron, 43, 585–593.CrossRefGoogle ScholarPubMed
Cooke, D. F., Taylor, C. S. R., Moore, T., & Graziano, M. S. A. (2003). Complex movements evoked by microstimulation of Area VIP. Proceedings of the National Academy of Sciences, 100, 6163–6168.CrossRefGoogle Scholar
Darwin, C. (1872). The expression of emotions in man and animals. London: John Murray.CrossRefGoogle Scholar
Desmurget, M., Song, Z., Mottolese, C., & Sirigu, A. (2013). Re-establishing the merits of electrical brain stimulation. Trends in Cognitive Sciences, 17, 442–449.CrossRefGoogle ScholarPubMed
Donoghue, J. P., Leibovic, S., & Sanes, J. N. (1992). Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles. Experimental Brain Research, 89, 1–19.CrossRefGoogle ScholarPubMed
Dosey, M. A., & Meisels, M. (1969). Personal space and self-protection. Journal of Personality and Social Psychology, 11, 93–97.CrossRefGoogle ScholarPubMed
Ferrier, D. (1874). Experiments on the brain of monkeys – No. 1. Proceedings of the Royal Society of London, 23, 409–430.Google Scholar
Foerster, O. (1936). The motor cortex of man in the light of Hughlings Jackson’s doctrines. Brain, 59, 135–159.CrossRefGoogle Scholar
Fogassi, L., Gallese, V., Fadiga, L., Luppino, G., Matelli, M., & Rizzolatti, G. (1996). Coding of peripersonal space in inferior premotor cortex (area F4). Journal of Neurophysiology, 76, 141–157.CrossRefGoogle ScholarPubMed
Fritsch, G., & Hitzig, E. (1870 [1960]). Uber die elektrishe Erregbarkeit des Grosshirns [On the electrical excitability of the cerebrum]. In G. von Bonin (Ed./transl.), Some papers on the cerebral cortex. Springfield, IL: Charles C Thomas Publisher, 73–96.Google Scholar
Fulton, J. F. (1938). Physiology of the nervous system. New York: Oxford University Press, 399–457.Google Scholar
Gentilucci, M., Fogassi, L., Luppino, G., Matelli, M., Camarda, R., & Rizzolatti, G. (1988). Functional organization of inferior area 6 in the macaque monkey.I. Somatotopy and the control of proximal movements. Experiments in Brain Research, 71, 475–490.CrossRefGoogle ScholarPubMed
Georgopoulos, A. P., Ashe, J., Smyrnis, N., & Taira, M. (1992). The motor cortex and the coding of force. Science, 256, 1692–1695.CrossRefGoogle ScholarPubMed
Georgopoulos, A. P., Kalaska, J. F., Caminiti, R., & Massey, J. T. (1982). On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. Journal of Neuroscience, 2, 1527–1537.CrossRefGoogle ScholarPubMed
Georgopoulos, A. P., Schwartz, A. B., & Kettner, R. E. (1986). Neuronal population coding of movement direction. Science, 233, 1416–1419.CrossRefGoogle ScholarPubMed
Gould, H. J. III, Cusick, C. G., Pons, T. P., & Kaas, J. H. (1986). The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys. Journal of Comparative Neurology, 247, 297–325.CrossRefGoogle ScholarPubMed
Graziano, M. S. A. (2006). The organization of behavioral repertoire in motor cortex. Annual Review of Neuroscience, 29, 105–134.CrossRefGoogle ScholarPubMed
Graziano, M. S. A. (2008). The intelligent movement machine: An ethological perspective on the primate motor system. Oxford: Oxford University Press.Google Scholar
Graziano, M. S. A., & Aflalo, T. N. (2007). Mapping behavioral repertoire onto the cortex. Neuron, 56, 239–251.CrossRefGoogle ScholarPubMed
Graziano, M. S. A., Aflalo, T. N. S., & Cooke, D. F. (2005). Arm movements evoked by electrical stimulation in the motor cortex of monkeys. Journal of Neurophysiology, 94, 4209–4223CrossRefGoogle ScholarPubMed
Graziano, M. S. A., & Cooke, D. F. (2006). Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia, 44, 845–859.CrossRefGoogle ScholarPubMed
Graziano, M. S. A., Cooke, D. F., Taylor, C. S. R., & Moore, T. (2004). Distribution of hand location in monkeys during spontaneous behavior. Experiments in Brain Research, 155, 30–36.CrossRefGoogle ScholarPubMed
Graziano, M. S. A., & Gandhi, S. (2000). Location of the polysensory zone in the precentral gyrus of anesthetized monkeys. Experiments in Brain Research, 135, 259–266.CrossRefGoogle ScholarPubMed
Graziano, M. S. A., Hu, X. T., & Gross, C. G. (1997). Visuo-spatial properties of ventral premotor cortex. Journal of Neurophysiology, 77, 2268–2292.CrossRefGoogle Scholar
Graziano, M. S. A., Taylor, C. S. R., & Moore, T. (2002). Complex movements evoked by microstimulation of precentral cortex. Neuron, 34, 841–851.CrossRefGoogle ScholarPubMed
Graziano, M. S. A., Yap, G. S., & Gross, C. G. (1994). Coding of visual space by pre-motor neurons. Science, 266, 1054–1057.CrossRefGoogle Scholar
Haiss, F., & Schwarz, C. (2005). Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex. Journal of Neuroscience, 25, 1579–1587.CrossRefGoogle ScholarPubMed
Hall, E. T. (1966). The hidden dimension. Garden City, New York: Anchor Books.Google Scholar
Harrison, T. C., Ayling, O. G., & Murphy, T. H. (2012). Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography. Neuron, 74, 397–409.CrossRefGoogle ScholarPubMed
Hediger, H. (1955). Studies of the psychology and behavior of captive animals in zoos and circuses. New York: Criterion Books.Google Scholar
Hess, W. R. (1957). Functional organization of the diencephalons. New York: Grune and Stratton.Google Scholar
Hoebel, B. G. (1969). Feeding and self-stimulation. Annals of the New York Academy of Sciences, 157, 758–778.CrossRefGoogle ScholarPubMed
Holdefer, R. N., & Miller, L. E. (2002). Primary motor cortical neurons encode functional muscle synergies. Experiments in Brain Research, 146, 233–243.CrossRefGoogle ScholarPubMed
Holt, D. J., Cassidy, B. S., Yue, X., Rauch, S. L., Boeke, E. A., et al. (2014). Neural correlates of personal space intrusion. Journal of Neuroscience, 34, 4123–4134.CrossRefGoogle ScholarPubMed
Hooff, J. van (1962). Facial expression in higher primates. Symposia of the Zoological Society of London, 8, 97–125.Google Scholar
Hooff, J. van (1972). A comparative approach to the phylogeny of laughter and smiling. In Hind, R. A. (Ed.), Non-verbal communication. Cambridge: Cambridge University Press, 209–241.Google Scholar
Horowitz, M. J., Duff, D. F., & Stratton, L. O. (1964). Body-buffer zone: Exploration of personal space. Archives of General Psychiatry, 11, 651–656.CrossRefGoogle ScholarPubMed
Kakei, S., Hoffman, D., & Strick, P. (1999). Muscle and movemet representations in the primary motor cortex. Science, 285, 2136–2139.CrossRefGoogle ScholarPubMed
King, M. B., & Hoebel, B. G. (1968). Killing elicited by brain stimulation in rats. Communications in Behavioral Biology, 2, 173–177.Google Scholar
Kwan, H. C., MacKay, W. A., Murphy, J. T., & Wong, Y. C. (1978). Spatial organization of precentral cortex in awake primates. II. Motor outputs. Journal of Neurophysiology, 41, 1120–1131.CrossRefGoogle ScholarPubMed
Macfarlane, N. B. W., & Graziano, M. S. A. (2009). Diversity of grip in Macaca mulatta. Experiments in Brain Research, 197, 255–268.CrossRefGoogle ScholarPubMed
Martin, J. H., Engber, D., & Meng, Z. (2005). Effect of forelimb use on postnatal development of the forelimb motor representation in primary motor cortex of the cat. Journal of Neurophysiology, 93, 2822–2831.CrossRefGoogle ScholarPubMed
Meier, J. D., Aflalo, T. N., Kastner, S., & Graziano, M. S. A. (2008). Complex organization of human primary motor cortex: A high-resolution fMRI study. Journal of Neurophysiology, 100, 1800–1812.CrossRefGoogle ScholarPubMed
Moran, D. W., & Schwartz, A. B. (1999). Motor cortical representation of speed and direction during reaching. Journal of Neurophysiology, 82, 2676–2692.CrossRefGoogle ScholarPubMed
Nudo, R. J., Milliken, G. W., Jenkins, W. M., & Merzenich, M. M. (1996). Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. Journal of Neurosciences, 16, 785–807.CrossRefGoogle ScholarPubMed
Overduin, S. A., d’Avella, A., Carmena, J. M., & Bizzi, E. (2012). Microstimulation activates a handful of muscle synergies. Neuron, 76, 1071–1077.CrossRefGoogle ScholarPubMed
Paninski, L., Fellows, M. R., Hatsopoulos, N. G., & Donoghue, J. P. (2004). Spatiotemporal tuning of motor cortical neurons for hand position and velocity. Journal of Neurophysiology, 91, 515–532.CrossRefGoogle ScholarPubMed
Park, M. C., Belhaj-Saif, A., Gordon, M., & Cheney, P. D. (2001). Consistent features in the forelimb representation of primary motor cortex in rhesus macaques. Journal of Neuroscience, 21, 2784–2792.CrossRefGoogle ScholarPubMed
Penfield, W., & Boldrey, E. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 60, 389–443.CrossRefGoogle Scholar
Penfield, W., & Rasmussen, T. (1950). The cerebral cortex of man: A clinical study of localization of function. New York: Macmillan.Google Scholar
Preuschoft, S. (1992). ‘Laughter’ and ‘smile’ in Barbary macaques (Macaca sylvanus). Ethology, 91, 220–236.CrossRefGoogle Scholar
Ramanathan, D., Conner, J. M., & Tuszynski, M. H. (2006). A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proceedings of the National Academy of Sciences USA, 103, 11370–11375.CrossRefGoogle ScholarPubMed
Rathelot, J. A., & Strick, P. L. (2006). Muscle representation in the macaque motor cortex: An anatomical perspective. Proceedings of the National Academy of Sciences USA, 103, 8257–8262.CrossRefGoogle ScholarPubMed
Reina, G. A., Moran, D. W., & Schwartz, A. B. (2001). On the relationship between joint angular velocity and motor cortical discharge during reaching. Journal of Neurophysiology, 85, 2576–2589.CrossRefGoogle ScholarPubMed
Rizzolatti, G., Scandolara, C., Matelli, M., & Gentilucci, M. (1981). Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behavioural Brain Research, 2, 147–163.CrossRefGoogle ScholarPubMed
Robinson, D. A. (1972). Eye movements evoked by collicular stimulation in the alert monkey. Vision Research, 12, 1795–1808.CrossRefGoogle ScholarPubMed
Robinson, D. A., & Fuchs, A. F. (1969). Eye movements evoked by stimulation of the frontal eye fields. Journal of Neurophysiology, 32, 637–648.CrossRefGoogle ScholarPubMed
Romo, R., Hernandez, A., Zainos, A., & Salinas, E. (1998). Somatosensory discrimination based on cortical microstimulation. Nature, 392, 387–390.CrossRefGoogle ScholarPubMed
Ross, M. D., Owren, M. J., & Zimmermann, E. (2010). The evolution of laughter in great apes and humans. Communicative and Integrative Biology, 3, 191–194.CrossRefGoogle ScholarPubMed
Salzman, C. D., Britten, K. H., & Newsome, W. T. (1990). Cortical microstimulation influences perceptual judgements of motion direction. Nature, 346, 174–177.CrossRefGoogle ScholarPubMed
Sambo, C. F., & Iannetti, G. D. (2013). Better safe than sorry? The safety margin surrounding the body is increased by anxiety. Journal of Neuroscience, 33, 14225–14230.CrossRefGoogle ScholarPubMed
Sanes, J. N., Donoghue, J. P., Thangaraj, V., Edelman, R. R., & Warach, S. (1995). Shared neural substrates controlling hand movements in human motor cortex. Science, 268, 1775–1777.CrossRefGoogle ScholarPubMed
Schieber, M. H., & Hibbard, L. S. (1993). How somatotopic is the motor cortex hand area? Science, 261, 489–492.CrossRefGoogle ScholarPubMed
Schiller, P. H., & Stryker, M. (1972). Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology, 35, 915–924.CrossRefGoogle ScholarPubMed
Scott, S. H., & Kalaska, J. F. (1997). Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. Journal of Neurophysiology, 77, 826–852.CrossRefGoogle ScholarPubMed
Sergio, L. E., & Kalaska, J. F. (2003). Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation. Journal of Neurophysiology, 89, 212–228.CrossRefGoogle ScholarPubMed
Sherrington, C. S. (1939). On the motor area of the cerebral cortex. In Denny-Brown, D. (Ed.), Selected writings of Sir Charles Sherrington. London: Hamish Hamilton Medical Books, 397–439.Google Scholar
Sommer, R. (1959). Studies in personal space. Sociometry, 22, 247–260.CrossRefGoogle Scholar
Stepniewska, I., Fang, P. C., & Kaas, J. H. (2005). Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos. Proceedings of the National Academy of Sciences USA, 102, 4878–4883.CrossRefGoogle ScholarPubMed
Stepniewska, I., Fang, P. C., (2009). Organization of the posterior parietal cortex in galagos: I. Functional zones identified by microstimulation. Journal of Comparative Neurology, 517, 765–782.CrossRefGoogle ScholarPubMed
Strick, P. L., & Preston, J. B. (1978). Multiple representation in the primate motor cortex. Brain Research, 154, 366–370.CrossRefGoogle ScholarPubMed
Teneggi, C., Canzoneri, E., di Pellegrino, G., & Serino, A. (2013). Social modulation of peripersonal space boundaries. Current Biology, 23, 406–411.CrossRefGoogle ScholarPubMed
Todorov, E. (2000). Direct cortical control of muscle activation in voluntary arm movements: A model. Nature Neuroscience, 3, 391–398.CrossRefGoogle ScholarPubMed
Townsend, B. R., Paninski, L., & Lemon, R. N. (2006). Linear encoding of muscle activity in primary motor cortex and cerebellum. Journal of Neurophysiology, 96, 2578–2592.CrossRefGoogle ScholarPubMed
Van Acker, G. M. III, Amundsen, S. L., Messamore, W. G., Zhang, H. Y., et al. (2013). Effective intracortical microstimulation parameters for evoking forelimb movements to stable spatial end-points from primary motor cortex. Journal of Neurophysiology, 110, 1180–1189.CrossRefGoogle ScholarPubMed
Woolsey, C. N., Settlage, P. H., Meyer, D. R., Sencer, W., Hamuy, T. P., & Travis, A. M. (1952). Pattern of localization in precentral and ‘supplementary’ motor areas and their relation to the concept of a premotor area. In Association for Research in Nervous and Mental Disease, Vol. 30. New York: Raven Press, 238–264.Google Scholar

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