Overlapping corticostriatal projections from the supplementary motor area and the primary motor cortex in the macaque monkey: An anterograde double labeling study

The purpose of the present study was to determine if the cortical efferents from homologous body regions of the supplementary motor area (SMA) and the primary motor cortex (MI) project to separate or to overlapping regions in the striatum. In order to investigate the dual corticostriatal projections, we employed an anterograde double labeling paradigm in which two tracers could be simultaneously detected in the same histological section. Prior to the injections, the forelimb representation in the two cortical motor areas was identified by using intracortical microstimulation in four Japanese monkeys (Macaca fuscata). Multiple injections of biotinylated dextran amine (BDA) were made into the forelimb regions of MI and wheat germ agglutinin conjugated horseradish peroxidase (WGA‐HRP) was injected into the arm region of the SMA. In additional animals, the tracers were reversed such that BDA was injected into the SMA and WGA‐HRP was injected into the MI. The tissue was processed sequentially using different chromogens in order to visualize both tracers in a single section. We analyzed the distribution of the ipsilateral anterograde label. The striatal labeling from each cortical area basically consisted of a wide band of patchy dense labeling interrupted by lighter labeling. The SMA striatal projections were located mainly within the putamen, distributing from the level of the anterior commissure to the most posterior extent of the putamen. At an intermediate level, the label spread obliquely from the ventrolateral edge of the putamen dorsomedially as far as the lateral edge of the caudate nucleus. The label from the MI was observed in comparable portions of the putamen, although the SMA projections were shifted more anterior and dorsomedial to the MI projections and the heaviest projections from the SMA and the MI were separately located. On the basis of the double anterograde labeling technique, we found considerable overlap mainly in the central portion of the putamen from the SMA and MI forelimb representation. These results suggest that the homologous body regions of the SMA and MI send widespread, and substantially overlapping projections, to portions of the striatum. © 1996 Wiley‐Liss, Inc.

[1]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[4]  H C Kwan,et al.  Spatial organization of precentral cortex in awake primates. II. Motor outputs. , 1978, Journal of neurophysiology.

[5]  R. Porter,et al.  Cells of origin and terminal distrubution of corticostriatal fibers arising in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[6]  D. Pandya,et al.  Striatal connections of the parietal association cortices in rhesus monkeys , 1993, The Journal of comparative neurology.

[7]  A. Graybiel,et al.  Distributed but convergent ordering of corticostriatal projections: analysis of the frontal eye field and the supplementary eye field in the macaque monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  H. Künzle Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[9]  E. Yeterian,et al.  Cortico-striate projections in the rhesus monkey: The organization of certain cortico-caudate connections , 1978, Brain Research.

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

[11]  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.

[12]  F. Olucha,et al.  A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP) , 1985, Journal of Neuroscience Methods.

[13]  M. Wiesendanger,et al.  Structural and functional definition of the motor cortex in the monkey (Macaca fascicularis) , 1982, The Journal of physiology.

[14]  Floris G. Wouterlood,et al.  The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy , 1993, Journal of Neuroscience Methods.

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

[16]  A. Graybiel,et al.  Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. , 1991, Journal of neurophysiology.

[17]  A. Graybiel,et al.  Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  B. Wainer,et al.  Stabilization of the tetramethylbenzidine (TMB) reaction product: application for retrograde and anterograde tracing, and combination with immunohistochemistry. , 1984, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[19]  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.

[20]  P. Strick,et al.  Multiple output channels in the basal ganglia. , 1993, Science.

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

[22]  S. T. Sakai,et al.  Comparison of cerebellothalamic and pallidothalamic projections in the monkey (Macaca fuscata): A double anterograde labeling study , 1996, The Journal of comparative neurology.

[23]  H. Gould,et al.  Topographic distribution of connections from the primary motor cortex to the corpus striatum in Aotus trivirgatus , 1991, The Journal of comparative neurology.

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

[25]  B. V. Updyke,et al.  Projection of the digit and wrist area of precentral gyrus to the putamen: Relation between topography and physiological properties of neurons in the putamen , 1985, Brain Research.

[26]  D. Pandya,et al.  Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys , 1991, The Journal of comparative neurology.

[27]  PL Strick,et al.  The origin of thalamic inputs to the "hand" representation in the primary motor cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  P. Goldman-Rakic,et al.  Topographic segregation of corticostriatal projections from posterior parietal subdivisions in the macaque monkey , 1991, Neuroscience.

[29]  M. P. Witter,et al.  Multiple anterograde tracing, combining Phaseolus vulgaris leucoagglutinin with rhodamine- and biotin-conjugated dextran amine , 1994, Journal of Neuroscience Methods.

[30]  J Tanji,et al.  Digit-muscle responses evoked from multiple intracortical foci in monkey precentral motor cortex. , 1989, Journal of neurophysiology.

[31]  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.

[32]  A. Vania Apkarian,et al.  Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey , 1992, Journal of Neuroscience Methods.

[33]  M. Inase,et al.  Thalamic distribution of projection neurons to the primary motor cortex relative to afferent terminal fields from the globus pallidus in the macaque monkey , 1995, The Journal of comparative neurology.

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

[35]  P. Goldman-Rakic,et al.  New frontiers in basal ganglia research , 1990, Trends in Neurosciences.