Organization of inputs from cingulate motor areas to basal ganglia in macaque monkey

The cingulate motor areas reside within regions lining the cingulate sulcus and are divided into rostral and caudal parts. Recent studies suggest that the rostral and caudal cingulate motor areas participate in distinct aspects of motor function: the former plays a role in higher‐order cognitive control of movements, whereas the latter is more directly involved in their execution. Here, we investigated the organization of cingulate motor areas inputs to the basal ganglia in the macaque monkey. Identified forelimb representations of the rostral and caudal cingulate motor areas were injected with different anterograde tracers and the distribution patterns of labelled terminals were analysed in the striatum and the subthalamic nucleus. Corticostriatal inputs from the rostral and caudal cingulate motor areas were located within the rostral striatum, with the highest density in the striatal cell bridges and the ventrolateral portions of the putamen, respectively. There was no substantial overlap between these input zones. Similarly, a certain segregation of input zones from the rostral and caudal cingulate motor areas occurred along the mediolateral axis of the subthalamic nucleus. It has also been revealed that corticostriatal and corticosubthalamic input zones from the rostral cingulate motor area considerably overlapped those from the presupplementary motor area, while the input zones from the caudal cingulate motor area displayed a large overlap with those from the primary motor cortex. The present results indicate that a parallel design underlies motor information processing in the cortico‐basal ganglia loop derived from the rostral and caudal cingulate motor areas.

[1]  A. Parent,et al.  Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry , 1995, Brain Research Reviews.

[2]  S. Haber,et al.  Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input , 1994, The Journal of comparative neurology.

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

[4]  J. Tanji,et al.  Neuronal activity in the primate supplementary, pre-supplementary and premotor cortex during externally and internally instructed sequential movements , 1994, Neuroscience Research.

[5]  K. Kiehl,et al.  Error processing and the rostral anterior cingulate: an event-related fMRI study. , 2000, Psychophysiology.

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

[7]  M. Inase,et al.  Organization of somatic motor inputs from the frontal lobe to the pedunculopontine tegmental nucleus in the macaque monkey , 2000, Neuroscience.

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

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

[10]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

[11]  J Tanji,et al.  Role for cells in the presupplementary motor area in updating motor plans. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[13]  R. Kawashima,et al.  A positron emission tomography study of self-paced finger movements at different frequencies , 1999, Neuroscience.

[14]  H. Kita,et al.  Excitatory Cortical Inputs to Pallidal Neurons Via the Subthalamic Nucleus in the Monkey , 2000 .

[15]  Atsushi Nambu,et al.  Somatotopic arrangement and corticocortical inputs of the hindlimb region of the primary motor cortex in the macaque monkey , 2001, Neuroscience Research.

[16]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[17]  Karl J. Friston,et al.  Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. , 1998, Journal of neurophysiology.

[18]  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.

[19]  A. Graybiel Building action repertoires: memory and learning functions of the basal ganglia , 1995, Current Opinion in Neurobiology.

[20]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[21]  S P Wise,et al.  The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Inase,et al.  Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex , 1998, Experimental Brain Research.

[24]  D. Joel,et al.  The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated , 1994, Neuroscience.

[25]  J. Tanji,et al.  Spatial distribution of cingulate cells projecting to the primary, supplementary, and pre-supplementary motor areas: a retrograde multiple labeling study in the macaque monkey , 2001, Neuroscience Research.

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

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

[28]  A. Graybiel,et al.  Role of Basal Ganglia in Sensory Motor Association Learning , 1995 .

[29]  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.

[30]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[31]  S. Wise The primate premotor cortex: past, present, and preparatory. , 1985, Annual review of neuroscience.

[32]  W. T. Thach,et al.  Basal ganglia intrinsic circuits and their role in behavior , 1993, Current Opinion in Neurobiology.

[33]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[34]  Masahiko Inase,et al.  Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area , 1997, Neuroscience Letters.

[35]  A. Dagher,et al.  Mapping the network for planning: a correlational PET activation study with the Tower of London task. , 1999, Brain : a journal of neurology.

[36]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[37]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[38]  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.

[39]  J. Morrison,et al.  Neurochemical, morphologic, and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey , 1996, The Journal of comparative neurology.

[40]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[41]  J. Joseph,et al.  Activity in the caudate nucleus of monkey during spatial sequencing. , 1995, Journal of neurophysiology.

[42]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

[43]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[44]  M. Inase,et al.  Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  Naomi Hasegawa,et al.  A cortical motor region that represents the cutaneous back muscles in the macaque monkey , 2000, Neuroscience Letters.

[46]  Peter L. Strick,et al.  Macro-organization of the circuits connecting the basal ganglia with the cortical motor areas , 1995 .

[47]  E. Procyk,et al.  Anterior cingulate activity during routine and non-routine sequential behaviors in macaques , 2000, Nature Neuroscience.

[48]  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.

[49]  O Hikosaka,et al.  Effects of local inactivation of monkey medial frontal cortex in learning of sequential procedures. , 1999, Journal of neurophysiology.

[50]  J. Tanji,et al.  A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. , 1992, Journal of neurophysiology.

[51]  P. Strick,et al.  Basal Ganglia ‘Loops’ with the Cerebral Cortex , 1995 .

[52]  K. Kurata Information processing for motor control in primate premotor cortex , 1994, Behavioural Brain Research.

[53]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[54]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[55]  J. Tanji The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[56]  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.

[57]  Jun Tanji,et al.  New concepts of the supplementary motor area , 1996, Current Opinion in Neurobiology.

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

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

[60]  O. Hikosaka,et al.  Differential roles of monkey striatum in learning of sequential hand movement , 1997, Experimental Brain Research.

[61]  Kae Nakamura,et al.  Neuronal activity in medial frontal cortex during learning of sequential procedures. , 1998, Journal of neurophysiology.

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

[63]  M. Inase,et al.  Origin of thalamocortical projections to the presupplementary motor area (pre-SMA) in the macaque monkey , 1996, Neurosciences research.

[64]  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.

[65]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[66]  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.

[67]  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.

[68]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[69]  Masahiko Inase,et al.  Corticostriatal input zones from the supplementary motor area overlap those from the contra- rather than ipsilateral primary motor cortex , 1998, Brain Research.

[70]  A. Parent,et al.  Anatomical aspects of information processing in primate basal ganglia , 1993, Trends in Neurosciences.

[71]  M. Inase,et al.  Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey , 1997, The Journal of comparative neurology.

[72]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[73]  Nikolaus R. McFarland,et al.  Convergent Inputs from Thalamic Motor Nuclei and Frontal Cortical Areas to the Dorsal Striatum in the Primate , 2000, The Journal of Neuroscience.

[74]  J Tanji,et al.  Overlapping corticostriatal projections from the supplementary motor area and the primary motor cortex in the macaque monkey: An anterograde double labeling study , 1996, The Journal of comparative neurology.

[75]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[76]  M. Inase,et al.  Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: comparison with the input zones from the supplementary motor area , 1999, Brain Research.

[77]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[78]  B. Feige,et al.  The Role of Higher-Order Motor Areas in Voluntary Movement as Revealed by High-Resolution EEG and fMRI , 1999, NeuroImage.

[79]  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.

[80]  O. Hikosaka,et al.  Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. , 1996, Journal of neurophysiology.

[81]  J Tanji,et al.  Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. , 1996, Journal of neurophysiology.

[82]  C. Gerfen,et al.  The frontal cortex-basal ganglia system in primates. , 1996, Critical reviews in neurobiology.

[83]  I. Hamada,et al.  A modified microsyringe for extracellular recording of neuronal activity , 1998, Neuroscience Research.