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Columnar Organization of the Motor Cortex: Direction of Movement

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Recent Advances on the Modular Organization of the Cortex

Abstract

The discovery by Vernon B. Mountcastle of the columnar organization of the cerebral cortex (Mountcastle VB, J Neurophysiol 20:408–434, 1957, Brain 120:701–722, 1997) was the single most important discovery of the twentieth century in cortical physiology. Not only did it serve as the framework for the orderly arrangement of knowledge concerning cortical organization and function (Edelman and Mountcastle, The mindful brain. MIT Press, Cambridge, MA, 1978) but also as a framework for exploring and investigating new ideas and for revisiting old ones about the organization of particular cortical areas. Here I review the history of facts and ideas about the organization of the motor cortex and discuss the evidence that the direction of movement is the principle governing motor cortical columnar organization.

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Notes

  1. 1.

    I argued in favor of the resurgence of this idea, playing the Devil’s advocate, at a meeting of the Neuroscience Research Program in La Jolla, CA in 2013. Dr. Edelman was incredulous and hardly believed his ears. Nevertheless, in his usual grand style, humor and compassion, he counter argued, and we had a lot of intellectual fun.

References

  • Abend W, Bizzi E, Morasso P (1982) Human arm trajectory formation. Brain 105:331–348

    Article  CAS  PubMed  Google Scholar 

  • Amirikian B, Georgopoulos AP (2003) Modular organization of directionally tuned cells in the motor cortex: is there a short-range order? Proc Natl Acad Sci U S A 100:12474–12479. doi:10.1073/pnas.2037719100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson CT, Sheets PL, Kiritani T, Shepherd GM (2010) Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat Neurosci 13:739–744. doi:10.1038/nn.2538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Apicella AJ, Wickersham IR, Seung HS, Shepherd GM (2012) Laminarly orthogonal excitation of fast-spiking and low-threshold-spiking interneurons in mouse motor cortex. J Neurosci 32:7021–7033. doi:10.1523/JNEUROSCI.0011-12.2012

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Asanuma H, Rosén I (1972) Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp Brain Res 14:243–256

    Article  CAS  PubMed  Google Scholar 

  • Asanuma H, Sakata H (1967) Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J Neurophysiol 30:35–54

    Google Scholar 

  • Caminiti R, Zeger S, Johnson PB, Urbano A, Georgopoulos AP (1985) Cortico-cortical efferent systems in the monkey: a quantitative spatial analysis of the tangential distribution of cells of origin. J Comp Neurol 241:405–419

    Article  CAS  PubMed  Google Scholar 

  • Caminiti R, Johnson PB, Urbano A, Georgopoulos AP, Zeger S (1988) Callosal and association neurons in the cortical space: a spectral analysis approach. Behav Brain Res 30:193–201

    Article  CAS  PubMed  Google Scholar 

  • Caminiti R, Johnson PB, Urbano A (1990) Making arm movements within different parts of space: dynamic aspects in the primate motor cortex. J Neurosci 10:2039–2058

    CAS  PubMed  Google Scholar 

  • Casanova MF (2007) The neuropathology of autism. Brain Pathol 17:422–433. doi:BPA100 [pii]

    Google Scholar 

  • Chadderdon GL, Mohan A, Suter BA, Neymotin SA, Kerr CC, Francis JT, Shepherd GM, Lytton WW (2014) Motor cortex microcircuit simulation based on brain activity mapping. Neural Comput 26:1239–1262. doi:10.1162/NECO_a_00602

    Article  PubMed  Google Scholar 

  • Christova P, Lewis SM, Jerde TA, Lynch JK, Georgopoulos AP (2011) True associations between resting fMRI time series based on innovations. J Neural Eng 8:046025. doi:10.1088/1741-2560/8/4/046025

    Article  CAS  PubMed  Google Scholar 

  • Collinger JL, Wodlinger B, Downey JE, Wang W, Tyler-Kabara EC, Weber DJ, McMorland AJ, Velliste M, Boninger ML, Schwartz AB (2013) High-performance neuroprosthetic control by an individual with tetraplegia. Lancet 381:557–564. doi:10.1016/S0140-6736(12)61816-9

    Article  PubMed Central  PubMed  Google Scholar 

  • Courtine G, Micera S, DiGiovanna J, Millan Jdel R (2013) Brain-machine interface: closer to therapeutic reality? Lancet 381:515–517. doi:10.1016/S0140-6736(12)62164-3

    Article  PubMed  Google Scholar 

  • Critchley J (1969) The parietal lobes. Hafner, New York

    Google Scholar 

  • Dow BM, Bauer R, Snyder AZ, Vautin RG (1984) Receptive fields and orientation shifts in foveal striate cortex of the awake macaque monkey. In: Edelman GM, Cowan WM, Gall WE (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 41–65

    Google Scholar 

  • Edelman GM, Mountcastle VB (1978) The mindful brain. MIT Press, Cambridge, MA

    Google Scholar 

  • Fetz E (1984) The representation of movement direction in the motor cortex: single cell and population studies. In: Edelman GM, Cowan WM, Gall WE (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 453–473

    Google Scholar 

  • Fitts PM, Deininger RL (1954) S-R compatibility: correspondence among paired elements within stimulus and response codes. J Exp Psychol 48:483–492

    Article  CAS  PubMed  Google Scholar 

  • Gatter KC, Powell TPS (1978) The intrinsic connections of the cortex of area 4 of the monkey. Brain 101:513–541

    Article  CAS  PubMed  Google Scholar 

  • Georgopoulos AP (1996) On the translation of directional motor cortical commands to activation of muscles via spinal interneuronal systems. Cogn Brain Res 3:151–155

    Article  CAS  Google Scholar 

  • Georgopoulos AP (2014) Cell directional spread determines accuracy, precision, and length of the neuronal population vector. Exp Brain Res 232:2391–2405. doi:10.1007/s00221-014-396-7

    Article  PubMed  Google Scholar 

  • Georgopoulos AP, Grillner S (1989) Visuomotor coordination in reaching and locomotion. Science 245:1209–1210

    Article  CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Massey JT (1991) Biomedical program research: the primate motor system. Johns Hopkins APL Tech Dig 12:105–114

    Google Scholar 

  • Georgopoulos AP, Stefanis C (2010) The motor cortical circuit. In: Shepherd G, Grillner S (eds) Brain microcircuits. Oxford University Press, New York, pp 39–45

    Chapter  Google Scholar 

  • Georgopoulos AP, Kalaska JF, Massey JT (1980) Cortical mechanisms of two-dimensional aiming arm movements. I. Aiming at different target locations. Soc Neurosci Abstr 6:156

    Google Scholar 

  • Georgopoulos AP, Kalaska JF, Massey JT (1981) Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. J Neurophysiol 46:725–743

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 2:1527–1537

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Caminiti R, Kalaska JF, Massey JT (1983) Spatial coding of movement: a hypothesis concerning the coding of movement direction by motor cortical populations. Exp Brain Res Suppl 7:327–336

    Google Scholar 

  • Georgopoulos AP, Kalaska JF, Crutcher MD, Caminiti R, Massey JT (1984) The representation of movement direction in the motor cortex: single cell and population studies. In: Edelman GM, Cowan WM, Gall WE (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 501–524

    Google Scholar 

  • Georgopoulos AP, Merchant H, Naselaris N, Amirikian B (2007) Mapping of the preferred direction in the motor cortex. Proc Natl Acad Sci U S A 104:11068–11072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233:1416–1419

    Article  CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Kettner RE, Schwartz AB (1988) Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population. J Neurosci 8:2928–2937

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Taira M, Lukashin A (1993) Cognitive neurophysiology of the motor cortex. Science 260:47–52

    Article  CAS  PubMed  Google Scholar 

  • Graziano MS, Taylor CS, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851. doi:S0896627302006980

    Article  CAS  PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York

    Google Scholar 

  • Jackson JH (1882) On some implications of dissolution of the nervous system. Medical Press and Circular, vol ii, p 411 (Reprinted in: Taylor J, Selected writings of John Hughlings Jackson, Stapes, London, UK, 1958, p. 29)

    Google Scholar 

  • Jankowska E (1975) Cortical motor representation in view of recent experiments on cortico-spinal relations. Acta Neurobiol Exp (Wars) 35:699–706

    CAS  Google Scholar 

  • Jankowska E, Padel Y, Tanaka R (1975) The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol Lond 249:617–636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601

    Article  CAS  PubMed  Google Scholar 

  • Jones EG, Powell TP (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93:793–820

    Article  CAS  PubMed  Google Scholar 

  • Kalaska JF, Caminiti R, Georgopoulos AP (1983) Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex. Exp Brain Res 51:247–260

    Article  CAS  PubMed  Google Scholar 

  • Kwan HC, MacKay WA, Murphy JT, Wong YC (1978) Spatial organization of precentral cortex in awake primates. II. Motor outputs. J Neurophysiol 41:1120–1131

    CAS  PubMed  Google Scholar 

  • Langheim FJ, Leuthold AC, Georgopoulos AP (2006) Synchronous dynamic brain networks revealed by magnetoencephalography. Proc Natl Acad Sci U S A 103:455–459. doi:10.1073/pnas.0509623102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lashley KS (1933) Integrative functions of the cerebral cortex. Physiol Rev 13:1–42

    Google Scholar 

  • Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG, Masmanidis SC, Taniguchi H, Huang ZJ, Zhang F, Boyden ES, Deisseroth K, Dan Y (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379–383. doi:10.1038/nature11312

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leuthold AC, Langheim FJ, Lewis SM, Georgopoulos AP (2005) Time series analysis of magnetoencephalographic data during copying. Exp Brain Res 164:411–422. doi:10.1007/s00221-005-2259-0

    Article  PubMed  Google Scholar 

  • Mahan MY, Georgopoulos AP (2013) Motor directional tuning across brain areas: directional resonance and the role of inhibition for directional accuracy. Front Neural Circ 7:92. doi:10.3389/fncir.2013.00092

    Google Scholar 

  • Mardia KV (1972) Statistics of directional data. Academic, New York

    Google Scholar 

  • Merchant H, Crowe DA, Fortes AF, Georgopoulos AP (2014) Cognitive modulation of local and callosal neural interactions in decision making. Front Neurosci 8:245. doi:10.3389/fnins.2014.00245

    Article  PubMed Central  PubMed  Google Scholar 

  • Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434

    CAS  PubMed  Google Scholar 

  • Mountcastle VB (1967) The problem of sensing and the neural coding of sensory events. In: Schmitt FO, Quarton G, Melnuchuk T (eds) The neurosciences: an intensive study program. Rockefeller University Press, New York, pp 393–407

    Google Scholar 

  • Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722

    Article  PubMed  Google Scholar 

  • Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871–908

    CAS  PubMed  Google Scholar 

  • Mountcastle VB, Motter BC, Andersen RA (1980) Some further observations of the functional properties of neurons in the parietal lobe of the waking monkey. Behav Brain Sci 3:485–534

    Article  Google Scholar 

  • Murphy JT, Kwan HC, MacKay WA, Wong YC (1982) Precentral unit activity correlated with angular components of a compound arm movement. Brain Res 246:141–145. doi:10.1016/0006-8993(82)90152-4

    Article  CAS  PubMed  Google Scholar 

  • Naselaris T, Merchant H, Amirikian B, Georgopoulos AP (2005) Spatial reconstruction of trajectories of an array of recording microelectrodes. J Neurophysiol 93:2318–2330. doi:10.1152/jn.00581.2004

    Article  PubMed  Google Scholar 

  • Naselaris T, Merchant H, Amirikian B, Georgopoulos AP (2006a) Large-scale organization of preferred directions in the motor cortex. I. Motor cortical hyperacuity for forward reaching. J Neurophysiol 96:3231–3236. doi:10.1152/jn.00487.2006

    Article  PubMed  Google Scholar 

  • Naselaris T, Merchant H, Amirikian B, Georgopoulos AP (2006b) Large-scale organization of preferred directions in the motor cortex. II. Analysis of local distributions. J Neurophysiol 96:3237–3247. doi:10.1152/jn.00488.2006

    Article  PubMed  Google Scholar 

  • Opris I, Casanova MF (2014) Prefrontal cortical minicolumn: from executive control to disrupted cognitive processing. Brain 137:1863–1875. doi:10.1093/brain/awt359

    Article  PubMed  Google Scholar 

  • Opris I, Hampson RE, Stanford TR, Gerhardt GA, Deadwyler SA (2011) Neural activity in frontal cortical cell layers: evidence for columnar sensorimotor processing. J Cogn Neurosci 23:1507–1521. doi:10.1162/jocn.2010.21534

    Article  PubMed Central  PubMed  Google Scholar 

  • Pellionisz A, Llinás R (1979) Brain modeling by tensor network theory and computer simulation. The cerebellum: distributed processor for predictive coordination. Neurosci 4:323–348. doi:10.1016/0306-4522(79)90097-6

    Article  CAS  Google Scholar 

  • Pellizzer G, Sargent P, Georgopoulos AP (1995) Motor cortical activity in a context-recall task. Science 269:702–705

    Article  CAS  PubMed  Google Scholar 

  • Pitts W, McCulloch WS (1947) How we know universals; the perception of auditory and visual forms. Bull Math Biophys 9:127–147

    Article  CAS  PubMed  Google Scholar 

  • Powell TP, Mountcastle VB (1959) Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull Johns Hopkins Hosp 105:133–162

    CAS  PubMed  Google Scholar 

  • Schwartz AB, Kettner RE, Georgopoulos AP (1988) Primate motor cortex and free arm movements to visual targets in three-dimensional space. I. Relations between single cell discharge and direction of movement. J Neurosci 8:2913–2927

    CAS  PubMed  Google Scholar 

  • Sherrington CS (1906) The integrative action of the nervous system. Yale University Press, New Haven

    Google Scholar 

  • Sherrington CS (1940) Man on his nature. Cambridge University Press, London

    Google Scholar 

  • Stefanis C, Jasper H (1964a) Intracellular microelectrode studies of antidromic responses in cortical pyramidal tract neurons. J Neurophysiol 27:828–854

    CAS  PubMed  Google Scholar 

  • Stefanis C, Jasper H (1964b) Recurrent collateral inhibition in pyramidal tract neurons. J Neurophysiol 27:855–877

    CAS  PubMed  Google Scholar 

  • Viviani P, Terzuolo C (1982) Trajectory determines movement dynamics. Neurosci 7:431–437. doi:10.1016/0306-4522(82)90277-9

    Article  CAS  Google Scholar 

  • Woolsey CN, Settlage PH, Meyer DR, Sencer W, Pinto Hamuy T, Travis AM (1952) Patterns of localization in precentral and “supplementary” motor areas and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis 30:238–264

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the American Legion Brain Sciences Chair and the US Department of Veterans Affairs.

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Correspondence to Apostolos P. Georgopoulos .

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Georgopoulos, A.P. (2015). Columnar Organization of the Motor Cortex: Direction of Movement. In: Casanova, M., Opris, I. (eds) Recent Advances on the Modular Organization of the Cortex. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9900-3_8

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