Interhemispheric connections of the ventral premotor cortex in a new world primate

This study describes the pattern of interhemispheric connections of the ventral premotor cortex (PMv) distal forelimb representation (DFL) in squirrel monkeys. Our objectives were to describe qualitatively and quantitatively the connections of PMv with contralateral cortical areas. Intracortical microstimulation techniques (ICMS) guided the injection of the neuronal tract tracers biotinylated dextran amine or Fast blue into PMv DFL. We classified the interhemispheric connections of PMv into three groups. Major connections were found in the contralateral PMv and supplementary motor area (SMA). Intermediate interhemispheric connections were found in the rostral portion of the primary motor cortex, the frontal area immediately rostral and ventral to PMv (FR), cingulate motor areas (CMAs), and dorsal premotor cortex (PMd). Minor connections were found inconsistently across cases in the anterior operculum (AO), posterior operculum/inferior parietal cortex (PO/IP), and posterior parietal cortex (PP), areas that consistently show connections with PMv in the ipsilateral hemisphere. Within‐case comparisons revealed that the percentage of PMv connections with contralateral SMA and PMd are higher than the percentage of PMv connections with these areas in the ipsilateral hemisphere; percentages of PMv connections with contralateral M1 rostral, FR, AO, and the primary somatosensory cortex are lower than percentages of PMv connections with these areas in the ipsilateral hemisphere. These studies increase our knowledge of the pattern of interhemispheric connection of PMv. They help to provide an anatomical foundation for understanding PMv's role in motor control of the hand and interhemispheric interactions that may underlie the coordination of bimanual movements. J. Comp. Neurol. 505:701–715, 2007. © 2007 Wiley‐Liss, Inc.

[1]  Kiyoshi Kurata,et al.  Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys , 1991, Neuroscience Research.

[2]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[3]  J. Talairach,et al.  Clinical consequences of corticectomies involving the supplementary motor area in man , 1977, Journal of the Neurological Sciences.

[4]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[5]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[6]  Scott Barbay,et al.  Ipsilateral connections of the ventral premotor cortex in a new world primate , 2006, The Journal of comparative neurology.

[7]  R. Lemon,et al.  Behaviour of neurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements , 2004, Experimental Brain Research.

[8]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[9]  R. Lemon,et al.  Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study , 2004, Experimental Brain Research.

[10]  S. Ghosh,et al.  A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. , 1995, Somatosensory & motor research.

[11]  R. Nudo,et al.  Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. , 1996, Journal of neurophysiology.

[12]  U. Jürgens,et al.  The efferent and afferent connections of the supplementary motor area , 1984, Brain Research.

[13]  J. Kaas,et al.  The distribution of commissural terminations in somatosensory areas I and II of the grey squirrel , 1981, The Journal of comparative neurology.

[14]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[15]  S. Barbay,et al.  Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. , 2006, Journal of neurophysiology.

[16]  G. Rizzolatti,et al.  Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey , 1985, Behavioural Brain Research.

[17]  P. Strick,et al.  Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas , 1979, Brain Research.

[18]  S. Swinnen.  Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

[19]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.

[20]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[21]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  S. Barbay,et al.  Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. , 2003, Journal of neurophysiology.

[23]  G. Rizzolatti,et al.  Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. , 1983, Brain : a journal of neurology.

[24]  L. Cohen,et al.  Transitions between dynamical states of differing stability in the human brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. W. Guillery.  On counting and counting errors , 2002, The Journal of comparative neurology.

[26]  S. Wise.  The Ventral Premotor Cortex, Corticospinal Region C, and the Origin of Primates , 2006, Cortex.

[27]  D. Boussaoud,et al.  Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways , 2002, Experimental Brain Research.

[28]  D. Boussaoud,et al.  Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study , 2005, BMC Neuroscience.

[29]  A. Reiner,et al.  Pathway tracing using biotinylated dextran amines , 2000, Journal of Neuroscience Methods.

[30]  M Lassonde,et al.  Neuropsychological alterations after split-brain surgery. , 1997, Journal of neurosurgical sciences.

[31]  M. Abercrombie.  Estimation of nuclear population from microtome sections , 1946, The Anatomical record.

[32]  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.

[33]  P. Rao.  Statistical Research Methods in the Life Sciences , 1997 .

[34]  J. Kaas,et al.  The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys , 1986, The Journal of comparative neurology.

[35]  M. Merzenich,et al.  Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  F. Gallyas.  Silver staining of myelin by means of physical development. , 1979, Neurological research.

[37]  R. Caminiti,et al.  Callosal connections of dorso‐lateral premotor cortex , 2003, The European journal of neuroscience.

[38]  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.

[39]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[40]  C. Brinkman.  Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  I. Kermadi,et al.  Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. , 2000, Somatosensory & motor research.

[42]  H. Lausberg,et al.  Callosal disconnection syndrome in a left-handed patient due to infarction of the total length of the corpus callosum , 1999, Neuropsychologia.

[43]  H. Forssberg,et al.  Neural networks for the coordination of the hands in time. , 2003, Journal of neurophysiology.

[44]  Youping Xiao,et al.  Projections from primary visual cortex to cytochrome oxidase thin stripes and interstripes of macaque visual area 2. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Honda,et al.  Neural correlates of the spontaneous phase transition during bimanual coordination. , 2006, Cerebral cortex.

[46]  P. Dixon,et al.  Topographically divergent and convergent connectivity between premotor and primary motor cortex. , 2006, Cerebral cortex.

[47]  Ann M. Stowe,et al.  Extensive Cortical Rewiring after Brain Injury , 2005, The Journal of Neuroscience.

[48]  J. Tanji,et al.  Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  Philip H. Ramsey.  Nonparametric Statistical Methods , 1974, Technometrics.

[50]  Neeraj Jain,et al.  Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys , 2001, The Journal of comparative neurology.

[51]  G. Rizzolatti,et al.  Somatotopic representation in inferior area 6 of the macaque monkey. , 1989, Brain, behavior and evolution.

[52]  K. Kurata,et al.  Reacquisition deficits in prism adaptation after muscimol microinjection into the ventral premotor cortex of monkeys. , 1999, Journal of neurophysiology.