Evidence that histochemically distinct zones of the primate substantia nigra pars compacta are related to patterned distributions of nigrostriatal projection neurons and striatonigral fibers

SummaryA marked histochemical compartmentalization is visible in the substantia nigra of the squirrel monkey in sections stained for acetylcholinesterase (AChE). In nigral regions containing tyrosine hydroxylase-positive neurons, there are AChE-poor and AChE-rich zones, and many of the AChE-poor zones have the form of narrow fingers extending ventrally into an AChE-rich matrix (Jimenez-Castellanos and Graybiel 1987b). The study reported here was carried out to determine whether this histochemical heterogeneity of the primate's substantia nigra is related to the known differentiation within its pars compacta of subdivisions projecting respectively to the caudate nucleus and to the putamen. Retrograde and anterograde labeling in the substantia nigra was elicited by tracer injections placed in the caudate nucleus or putamen and was plotted in relation to patterns of AChE staining and tyrosine hydroxylase immunostaining. Much of the labeling observed was organized according to borders visible with AChE histochemistry: labeled nigral neurons (and afferent fibers) tended to be clustered precisely within the AChE-poor ventrally-extending fingers or to be situated outside these zones. However, projection neurons in these ventrally-extending fingers were not exclusively related either to the caudate nucleus or to the putamen. After injections in the caudate nucleus, labeled neurons were predominantly in the AChE-poor fingers in some cases, but predominantly in AChE-rich nigral zones outside them in other cases. Labeling in and out of the ventrally-extending fingers, and along the edges of the fingers, also occurred following different tracer injections in the putamen. These findings confirm the independent clustering of nigrostriatal neurons projecting respectively to the caudate nucleus and to the putamen. The plan of nigrostriatal connections additionally appears concordant with the histochemical compartmentalization of the substantia nigra that can be detected with acetylthiocholinesterase histochemistry.

[1]  J. Olszewski,et al.  Cytoarchitecture of the Human Brain Stem , 1955 .

[2]  J. Szabo,et al.  Topical distribution of the striatal efferents in the monkey , 1962 .

[3]  T. Kusama.  [Fiber connections of the basal ganglia]. , 1966, No to shinkei = Brain and nerve.

[4]  A. Parent,et al.  Cholinesterasic striatopallidal and striatonigral efferents in the cat and the monkey. , 1970, Brain research.

[5]  M B Carpenter,et al.  Nigrostriatal and nigrothalamic fibers in the rhesus monkey , 1972, The Journal of comparative neurology.

[6]  A. Hendrickson,et al.  The autoradiographic demonstration of axonal connections in the central nervous system. , 1972, Brain research.

[7]  W. Nauta,et al.  Connections of the basal ganglia and of the cerebellum. , 1974, Confinia neurologica.

[8]  R. Hassler.  Fiber connections within the extrapyramidal system. , 1974, Confinia neurologica.

[9]  T. Ho¨kfelt,et al.  Retrograde peroxidase tracing of neurons combined with transmitter histochemistry , 1975, Brain Research.

[10]  Carpenter Mb.  Anatomical organization of the corpus striatum and related nuclei. , 1976 .

[11]  M. Carpenter.  Anatomical organization of the corpus striatum and related nuclei. , 1976, Research publications - Association for Research in Nervous and Mental Disease.

[12]  A. Parent,et al.  Morphological characteristics of acetylcholinesterase-containing neurons in the CNS of DFP-treated monkeys Part 2. Diencephalic and medial telencephalic structures , 1977, Journal of the Neurological Sciences.

[13]  A. Parent,et al.  Morphological characteristics of the acetylcholin-esterase-containing neurons in the CNS of DFP-treated monkeys Part 1. Extrapyramidal and related structures , 1977, Journal of the Neurological Sciences.

[14]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum , 1978, The Journal of comparative neurology.

[15]  H. Künzle.  An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. , 1978, Brain, behavior and evolution.

[16]  G. Aghajanian,et al.  Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra , 1978, Brain Research.

[17]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[18]  C. W. Ragsdale,et al.  Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[19]  ACETYLCHOLINESTERASE IS SYNTHESIZED AND TRANSPORTED BY DOPAMINE NEURONS IN PARS COMPACTA OF THE SUBSTANTIA NIGRA: FUNCTIONAL SIGNIFICANCE AND HISTOCHEMICAL CORRELATIONS ON THE SAME BRAIN SECTION , 1979 .

[20]  C. Harper,et al.  Superior sensitivity of conjugates of horseradish peroxidase with wheat germ agglutinin for studies of retrograde axonal transport. , 1979, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[21]  J. Szabo.  Strionigral and Nigrostriatal Connections , 1979 .

[22]  L. Butcher,et al.  The localization of acetylcholinesterase in the corpus striatum and substantia nigra of the rat following kainic acid lesion of the corpus striatum: A biochemical and histochemical study , 1979, Neuroscience.

[23]  J. Szabo.  Organization of the ascending striatal afferents in monkeys , 1980, The Journal of comparative neurology.

[24]  T. Hattori,et al.  Is there a non-dopaminergic nigrostriatal pathway? , 1981, Neuroscience.

[25]  Z. Henderson.  Ultrastructure and acetylcholinesterase content of neurones forming connections between the striatum and substantia nigra of rat , 1981, The Journal of comparative neurology.

[26]  Jonathan K. Crane,et al.  Non-dopaminergic nigrostriatal pathway , 1981, Brain Research.

[27]  A. Parent,et al.  The subcortical afferents to caudate nucleus and putamen in primate: A fluorescence retrograde double labeling study , 1983, Neuroscience.

[28]  M. Giguére,et al.  Comparative morphology of the substantia nigra and ventral tegmental area in the monkey, cat and rat , 1983, Brain Research Bulletin.

[29]  J. Yelnik,et al.  Localization of nigrostriatal, nigrothalamic and nigrotectal neurons in ventricular coordinates in macaques , 1984, Neuroscience.

[30]  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.

[31]  L. Schmued,et al.  Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties , 1986, Brain Research.

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

[33]  A. Parent,et al.  Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus) , 1986, Neuroscience.

[34]  S. Greenfield,et al.  Release of acetylcholinesterase in the rat nigrostriatal pathway: Relation to receptor activation and firing rate , 1986, Neuroscience.

[35]  A. Graybiel,et al.  Subdivisions of the dopamine-containing A8-A9-A10 complex identified by their differential mesostriatal innervation of striosomes and extrastriosomal matrix , 1987, Neuroscience.

[36]  J. Schneider,et al.  Basal ganglia and behavior : sensory aspects of motor functioning , 1987 .

[37]  S. Greenfield,et al.  Does the substantia nigra have a cholinergic innervation? , 1987, Neuroscience Letters.

[38]  A. Graybiel,et al.  Subdivisions of the primate substantia nigra pars compacta detected by acetylcholinesterase histochemistry , 1987, Brain Research.

[39]  T. Blackstad,et al.  Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[40]  E. Scarnati,et al.  A microiontophoretic study on the nature of the putative synaptic neurotransmitter involved in the pedunculopontine-substantia nigra pars compacta excitatory pathway of the rat , 2004, Experimental Brain Research.