Neural activity correlated with the preparation and execution of visually guided arm movements in the cingulate motor area of the monkey

Abstract. Recent anatomical and physiological studies have suggested that parts of the cingulate cortex are involved in the control of movement . These areas have been collectively termed the cingulate motor area (CMA). Currently almost nothing is known, however, about how neurons in the CMA actually participate in the control of movement. Therefore, we investigated the role of cells in the dorsal and ventral banks of the CMA (CMAd and CMAv, respectively) in the preparation and execution of visually guided arm movements. We recorded the activity of neurons while a monkey performed a visually guided, two-dimensional instructed delay task. A monkey was required to operate a joystick that moved a cursor from a centrally located hold target to one of four peripheral targets. Neurons were classified as exhibiting preparatory activity if the neural discharge during the postinstruction delay period was significantly higher than the preinstruction activity. Neurons were classified as exhibiting movement activity if the neural discharge was significantly elevated around the time of the movement. Of the 115 task-related neurons studied, 18 (16%) exhibited only preparatory activity, 48 (42%) exhibited only movement activity, and 49 (43%) exhibited both preparatory and movement activity. Neurons were further classified in terms of their directional tuning. For 51% of neurons with preparatory activity, that activity was directional. A significantly larger proportion of movement-related activity was directional (78%). For neurons with both directional preparatory and movement activity, the preferred directions were highly correlated (r=0.83). The median onset of movement activity was 10 ms before the beginning of movement (range –200 to 200 ms). The patterns and directionality of task-related activity of CMA neurons observed in this study are similar to those previously reported for other cortical motor areas. Together, these data provide preliminary evidence that neurons in CMAd and CMAv play a role in both the preparation and execution of visually guided arm movements.

[1]  S. Wise,et al.  Neuronal activity preceding directional and nondirectional cues in the premotor cortex of rhesus monkeys. , 1988, Somatosensory & motor research.

[2]  G. Rizzolatti,et al.  Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: An intracortical microstimulation study in the macaque monkey , 1991, The Journal of comparative neurology.

[3]  J Tanji,et al.  Neuronal activity in the ventral part of premotor cortex during target-reach movement is modulated by direction of gaze. , 1997, Journal of neurophysiology.

[4]  J. Kalaska,et al.  Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. , 1994, Journal of neurophysiology.

[5]  M. Hallett,et al.  Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. , 1999, Journal of neurophysiology.

[6]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[7]  K Zilles,et al.  Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. , 1996, Advances in neurology.

[8]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[9]  I. Darian‐Smith,et al.  Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. , 1994, Cerebral cortex.

[10]  G. Rizzolatti,et al.  Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey , 1991, The Journal of comparative neurology.

[11]  Richard S. J. Frackowiak,et al.  Multiple nonprimary motor areas in the human cortex. , 1997, Journal of neurophysiology.

[12]  G E Alexander,et al.  Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. , 1997, Journal of neurophysiology.

[13]  P. Strick,et al.  Cingulate Motor Areas , 1993 .

[14]  J. Tanji,et al.  Rostrocaudal distinction of the dorsal premotor area based on oculomotor involvement. , 2000, Journal of neurophysiology.

[15]  Brent A. Vogt,et al.  Structural Organization of Cingulate Cortex: Areas, Neurons, and Somatodendritic Transmitter Receptors , 1993 .

[16]  P. Strick,et al.  Medial wall motor areas and skeletomotor control , 1992, Current Opinion in Neurobiology.

[17]  M. Inase,et al.  Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements. , 1991, Journal of neurophysiology.

[18]  G E Alexander,et al.  Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[19]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[20]  R. Morecraft,et al.  Segregated parallel inputs to the brachial spinal cord from the cingulate motor cortex in the monkey. , 1997, Neuroreport.

[21]  Andrew R. Mitz,et al.  Eye-movement representation in the frontal lobe of rhesus monkeys , 1989, Neuroscience Letters.

[22]  S. Wise,et al.  Effects of attention on visuomotor activity in the premotor and prefrontal cortex of a primate. , 1993, Somatosensory & motor research.

[23]  K. Toyoshima,et al.  Exact cortical extent of the origin of the corticospinal tract (CST) and the quantitative contribution to the CST in different cytoarchitectonic areas. A study with horseradish peroxidase in the monkey. , 1982, Journal fur Hirnforschung.

[24]  P. Goldman-Rakic,et al.  Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. , 1991, Cerebral cortex.

[25]  G. E. Alexander,et al.  Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. , 1997, Journal of neurophysiology.

[26]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[28]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. II. Responses to movement triggering vs. nontriggering sensory signals. , 1985, Journal of neurophysiology.

[29]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  K. Kurata,et al.  Premotor cortex of monkeys: set- and movement-related activity reflecting amplitude and direction of wrist movements. , 1993, Journal of neurophysiology.

[31]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[32]  G. E. Alexander,et al.  Preparation for movement: neural representations of intended direction in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[33]  J Tanji,et al.  Input organization of distal and proximal forelimb areas in the monkey primary motor cortex: A retrograde double labeling study , 1993, The Journal of comparative neurology.

[34]  P. Strick,et al.  Activation on the medial wall during remembered sequences of reaching movements in monkeys. , 1997, Journal of neurophysiology.

[35]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[36]  F Bremmer,et al.  Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey. , 1998, Journal of neurophysiology.

[37]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

[39]  M. Honda,et al.  Both primary motor cortex and supplementary motor area play an important role in complex finger movement. , 1993, Brain : a journal of neurology.

[40]  B. Vogt,et al.  Connections of the Monkey Cingulate Cortex , 1993 .

[41]  A. M. Smith,et al.  Comparison of the neuronal activity in the SMA and the ventral cingulate cortex during prehension in the monkey. , 1997, Journal of neurophysiology.

[42]  J. Tanji,et al.  Supplementary motor area: neuronal response to motor instructions. , 1980, Journal of neurophysiology.

[43]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[44]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[45]  E. Batschelet Circular statistics in biology , 1981 .

[46]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[47]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  M. Hallett,et al.  Frontal and parietal networks for conditional motor learning: a positron emission tomography study. , 1997, Journal of neurophysiology.

[49]  G. V. Van Hoesen,et al.  Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey , 1993, The Journal of comparative neurology.

[50]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[51]  A. M. Smith,et al.  Input-output properties of hand-related cells in the ventral cingulate cortex in the monkey. , 1995, Journal of neurophysiology.