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Participation of primary motor cortical neurons in a distributed network during maze solution: representation of spatial parameters and time-course comparison with parietal area 7a

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Traditionally, primary motor cortex (M1) has been thought to be involved solely in planning and generating movements. Recent evidence suggests that the arm area of M1 plays a role in other functions, such as the representation of serial order (Pellizzer et al. 1995, Science 269:702–705; Carpenter et al. 1999, Science 283:1752–1757) and spatial processing (Georgopoulos et al. 1989, Science 243:234–236). Previous studies of such cognitive processes have used tasks in which a directed arm movement was required, raising a question as to whether this brain area is involved in cognitive processing per se, or whether such cognitive signals may be gated into the arm area of M1 only when arm movements are required. To study this question, we developed a task that required a spatial analysis of a complex visual stimulus, but required no arm movement as a response. In this task, monkeys were shown an octagonal maze. After an imposed delay of 2 to 2.5 s, they indicated whether a path that emanated from the center of the maze exited at the perimeter (exit maze) or terminated within the maze (no-exit maze) by pressing a pedal with their left or right foot, respectively. We recorded from 785 cells from the arm area of M1 from two monkeys during the delay period of the maze task. We found that cell activity was influenced by both the exit status and the direction of the path, beginning soon after the maze was displayed. This activity was not related to the activation of arm muscles, suggesting that the directional signals observed represented abstract spatial aspects of maze processing. Finally, we compared maze-related activity of M1 neurons with those recorded from posterior parietal area 7a, reported previously (Crowe et al. 2004). Interestingly, cells from each area exhibited similar properties. Both the exit status and path direction were encoded by cells in M1 and 7a, although to different extents. An analysis of the time-course of the neural representation of these factors revealed that area 7a and M1 begin to encode these factors at the same time, suggesting these brain areas are part of a distributed system performing the spatial computations involved in maze solution.

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References

  • Alexander GE, Crutcher MD (1990) Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. J Neurophysiol 64:164–178

    CAS  PubMed  Google Scholar 

  • Barash S, Bracewell RM, Fogassi L, Gnadt JW, Andersen RA (1991) Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a. J Neurophysiol 66:1095–1108

    CAS  PubMed  Google Scholar 

  • Beisteiner R, Hollinger P, Lindinger G, Lang W, Berthoz A (1995) Mental representations of movements. Brain potentials associated with imagination of hand movements. Electroencephalogr Clin Neurophysiol 96:183–193

    CAS  PubMed  Google Scholar 

  • Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13:400–404

    Article  CAS  PubMed  Google Scholar 

  • Carpenter AF, Georgopoulos AP, Pellizzer G (1999) Motor cortical encoding of serial order in a context-recall task. Science 283:1752–1757

    CAS  PubMed  Google Scholar 

  • Chafee MV, Averbeck BB, Crowe DA, Georgopoulos AP (2002) Impact of path parameters on maze solution time. Arch Ital Biol 140:247–251

    CAS  PubMed  Google Scholar 

  • Crowe DA, Averbeck BB, Chafee MV, Anderson JH, Georgopoulos AP (2000) Mental maze solving. J Cogn Neurosci 12:813–827

    Article  CAS  PubMed  Google Scholar 

  • Crowe DA, Chafee MV, Averbeck BB, Georgopoulos AP (2004) Neural activity in primate parietal area 7a related to spatial analysis of visual mazes. Cereb Cortex 14:23–34

    Article  PubMed  Google Scholar 

  • Fuchs AF, Robinson DA (1966) A method for measuring horizontal and vertical eye movement chronically in the monkey. J Appl Physiol 21:1068–1070

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP (2000) Neural aspects of cognitive motor control. Curr Opin Neurobiol 10:238–241

    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, Lurito JT, Petrides M, Schwartz AB, Massey JT (1989) Mental rotation of the neuronal population vector. Science 243:234–236

    CAS  PubMed  Google Scholar 

  • Gnadt JW, Andersen RA (1988) Memory related motor planning activity in posterior parietal cortex of macaque. Exp Brain Res 70:216–220

    CAS  PubMed  Google Scholar 

  • Gold JI, Shadlen MN (2000) Representation of a perceptual decision in developing oculomotor commands. Nature 404:390–394

    Article  CAS  PubMed  Google Scholar 

  • Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Mountcastle VB, Plum F, Geiger SR (eds) Handbook of physiology. The nervous system. higher functions of the brain, sect 1, vol V, chap 9. American Physiological Society, Bethesda MD, pp 373–417

  • Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Miyachi S, Doya K (1999) Parallel neural networks for learning sequential procedures. Trends Neurosci 22:464–471

    CAS  PubMed  Google Scholar 

  • Hocherman S, Wise SP (1991) Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys. Exp Brain Res 83:285–302

    CAS  PubMed  Google Scholar 

  • Ito M, Gilbert CD (1999) Attention modulates contextual influences in the primary visual cortex of alert monkeys. Neuron 22:593–604

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Kustov AA, Robinson DL (1996) Shared neural control of attentional shifts and eye movements. Nature 384:74–77

    CAS  PubMed  Google Scholar 

  • Lang W, Cheyne D, Hollinger P, Gerschlager W, Lindinger G (1996) Electric and magnetic fields of the brain accompanying internal simulation of movement. Brain Res Cogn Brain Res 3:125–129

    Article  CAS  PubMed  Google Scholar 

  • Lebedev MA, Wise SP (2001) Tuning for the orientation of spatial attention in dorsal premotor cortex. Eur J Neurosci 13:1002–1008

    Article  CAS  PubMed  Google Scholar 

  • Lee D, Port NL, Kruse W, Georgopoulos AP (1998) Neuronal population coding: multielectrode recordings in primate cerebral cortex. In: Eichenbaum H, Davis J (eds) Neuronal ensembles: strategies for recording and decoding. Wiley, New York, pp 117–136

  • Lotze M, Montoya P, Erb M, Hulsmann E, Flor H, Klose U, Birbaumer N, Grodd W (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci 11:491–501

    CAS  PubMed  Google Scholar 

  • Lurito JT, Georgakopoulos T, Georgopoulos AP (1991) Cognitive spatial-motor processes. 7. The making of movements at an angle from a stimulus direction: studies of motor cortical activity at the single cell and population levels. Exp Brain Res 87:562–580

    CAS  PubMed  Google Scholar 

  • Lynch JC, Mountcastle VB, Talbot WH, Yin TC (1977) Parietal lobe mechanisms for directed visual attention. J Neurophysiol 40:362–389

    Google Scholar 

  • Merchant H, Battaglia-Mayer A, Georgopoulos AP (2001) Effects of optic flow in motor cortex and area 7a. J Neurophysiol 86:1937–1954

    CAS  PubMed  Google Scholar 

  • Moore T, Fallah M (2001) Control of eye movements and spatial attention. Proc Natl Acad Sci USA 98:1273–1276

    CAS  PubMed  Google Scholar 

  • Moran J, Desimone R (1985) Selective attention gates visual processing in the extrastriate cortex. Science 229:782–784

    CAS  PubMed  Google Scholar 

  • Motter BC (1993) Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol 70:909–919

    CAS  PubMed  Google Scholar 

  • Mountcastle VB, Reitboeck HJ, Poggio GF, Steinmetz MA (1991) Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey. J Neurosci Methods 36:77–84

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Riehle A (1991) Visually induced signal-locked neuronal activity changes in precentral motor areas of the monkey: hierarchical progression of signal processing. Brain Res 540:131–137

    CAS  PubMed  Google Scholar 

  • Robinson DL, Goldberg ME, Stanton GB (1978) Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. J Neurophysiol 41:910–932

    CAS  PubMed  Google Scholar 

  • Roelfsema PR, Lamme VA, Spekreijse H (1998) Object-based attention in the primary visual cortex of the macaque monkey. Nature 395:376–381

    CAS  PubMed  Google Scholar 

  • Salinas E, Romo R (1998) Conversion of sensory signals into motor commands in primary motor cortex. J Neurosci 18:499–511

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tanji J (2001) Sequential organization of multiple movements: Involvement of cortical motor areas. Annu Rev Neurosci 24:631–651

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Apostolos P. Georgopoulos.

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Crowe, D.A., Chafee, M.V., Averbeck, B.B. et al. Participation of primary motor cortical neurons in a distributed network during maze solution: representation of spatial parameters and time-course comparison with parietal area 7a. Exp Brain Res 158, 28–34 (2004). https://doi.org/10.1007/s00221-004-1876-3

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