Distribution of limbic system-associated membrane protein immunoreactivity in primate basal ganglia

The limbic system-associated membrane protein is a 64,000-68,000 mol.wt molecule known to be preferentially expressed by neurons in limbic structures of rats and cats. The present immunohistochemical study describes the distribution of this protein in the basal ganglia of Macaca fascicularis. The ventral striatum of the cynomolgus monkey displays a very intense immunostaining, whereas the dorsal striatum is much more weakly stained, except for some small zones scattered in the caudate nucleus and, to a lesser extent, in the putamen. These protein-rich zones are in register with striosomes, as visualized on adjacent sections immunostained for calbindin. At pallidal levels, immunostaining for the protein is observed only in the subcommissural regions, at the ventromedial tip of the internal pallidum, and in the caudoventral portion of the external pallidum. At nigral levels, the immunostaining is highly heterogeneous with a marked decreasing rostrocaudal gradient. The staining is most intense in nigral regions that receive striatal inputs and are enriched with calbindin. Nigral sectors populated by dopaminergic neurons, as visualized on adjacent sections immunostained for tyrosine hydroxylase, are largely devoid of immunoreactivity. In contrast, the immunostaining is uniformly intense in the ventral tegmental area. This study provides the first neuroanatomical evidence for teh existence of the limbic system-associated membrane protein in primate brain. It reveals that this glycoprotein is distributed in a highly heterogeneous manner in primate basal ganglia, where it preferentially labels regions that are anatomically and functionally linked to the limbic system.

[1]  D. Amaral,et al.  The amygdalostriatal projections in the monkey. An anterograde tracing study , 1985, Brain Research.

[2]  A. Graybiel Neurotransmitters and neuromodulators in the basal ganglia , 1990, Trends in Neurosciences.

[3]  D. Price,et al.  The bed nucleus‐amygdala continuum in human and monkey , 1991, The Journal of comparative neurology.

[4]  F. Keller,et al.  Developmental and regeneration-associated regulation of the limbic system associated membrane protein in explant cultures of the rat brain , 1989, Neuroscience.

[5]  A. Parent,et al.  Complementary Distribution of Calbindin D‐28k and Parvalbumin in the Basal Forebrain and Midbrain of the Squirrel Monkey , 1991, The European journal of neuroscience.

[6]  C. W. Ragsdale,et al.  The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histochemistry , 1981, Brain Research.

[7]  S. Haber,et al.  Primate striatonigral projections: A comparison of the sensorimotor‐related striatum and the ventral striatum , 1994, The Journal of comparative neurology.

[8]  D. Amaral,et al.  An autoradiographic study of the projections of the central nucleus of the monkey amygdala , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  P. Levitt,et al.  Heterogeneous distribution of the limbic system-associated membrane protein in the caudate nucleus and substantia nigra of the cat , 1991, Neuroscience.

[10]  T. Jessell,et al.  Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes , 1994, Cell.

[11]  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.

[12]  M J Bastiani,et al.  Cell recognition during neuronal development. , 1984, Science.

[13]  Paul D. MacLean,et al.  An Explanation of Behavior. (Book Reviews: The Triune Brain in Evolution. Role in Paleocerebral Functions.) , 1990 .

[14]  M. Cassell,et al.  Neuronal architecture in the rat central nucleus of the amygdala: A cytological, hodological, and immunocytochemical study , 1986, The Journal of comparative neurology.

[15]  L. Heimer,et al.  New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata , 1988, Neuroscience.

[16]  P. Levitt,et al.  Cerebral cortical progenitors are fated to produce region-specific neuronal populations. , 1993, Cerebral cortex.

[17]  S. Haber,et al.  Topographic organization of the ventral striatal efferent projections in the rhesus monkey: An anterograde tracing study , 1990, The Journal of comparative neurology.

[18]  J. Johnston Further contributions to the study of the evolution of the forebrain , 1923 .

[19]  J. Price,et al.  A description of the amygdaloid complex in the rat and cat with observations on intra‐amygdaloid axonal connections , 1978, The Journal of comparative neurology.

[20]  R. Kötter,et al.  The limbic system: a review of its empirical foundation , 1992, Behavioural Brain Research.

[21]  D. Price,et al.  The striatal mosaic in primates: Patterns of neuropeptide immunoreactivity differentiate the ventral striatum from the dorsal striatum , 1991, Neuroscience.

[22]  Peter W. Kalivas,et al.  The Basal Forebrain , 1991, Advances in Experimental Medicine and Biology.

[23]  Cathleen Conzales,et al.  Amygdalonigral pathway: An anterograde study in the rat with Phaseolus vulgaris leucoagglutinin (PHA‐L) , 1990, The Journal of comparative neurology.

[24]  A. Parent Extrinsic connections of the basal ganglia , 1990, Trends in Neurosciences.

[25]  P. Levitt,et al.  Regulation of regional differences in the differentiation of cerebral cortical neurons by EGF family-matrix interactions. , 1995, Development.

[26]  S. Hsu,et al.  Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[27]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

[28]  A. Graybiel,et al.  Heterogeneous development of calbindin‐D28K expression in the striatal matrix , 1992, The Journal of comparative neurology.

[29]  S. N. Haber,et al.  The organization of midbrain projections to the ventral striatum in the primate , 1994, Neuroscience.

[30]  C. W. Ragsdale,et al.  Fibers from the basolateral nucleus of the amygdala selectively innervate striosomes in the caudate nucleus of the cat , 1988, The Journal of comparative neurology.

[31]  L. Heimer,et al.  Ventral striatum and ventral pallidum Components of the motor system? , 1982, Trends in Neurosciences.

[32]  A. Norman,et al.  Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. , 1990, Cell calcium.

[33]  S. Christakos,et al.  Ultrastructural localization of immunoreactive calbindin‐D28k in the rat and monkey basal ganglia, including subcellular distribution with colloidal gold labeling , 1989, The Journal of comparative neurology.

[34]  P. Levitt,et al.  The limbic system-associated membrane protein (LAMP) selectively mediates interactions with specific central neuron populations. , 1995, Development.

[35]  P. Levitt,et al.  A unique membrane protein is expressed on early developing limbic system axons and cortical targets , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  B. Lewin On neuronal specificity and the molecular basis of perception , 1994, Cell.

[37]  W. Nauta,et al.  An intricately patterned prefronto‐caudate projection in the rhesus monkey , 1977, The Journal of comparative neurology.

[38]  R. McKay,et al.  Monoclonal antibodies distinguish identifiable neurones in the leech , 1981, Nature.

[39]  S. Hockfield,et al.  A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[40]  L. Heimer,et al.  Piecing together the puzzle of basal forebrain anatomy. , 1991, Advances in experimental medicine and biology.

[41]  Robert L. Isaacson,et al.  A fuzzy limbic system , 1992, Behavioural Brain Research.

[42]  J. Donoghue,et al.  Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat , 1986, Brain Research.

[43]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

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

[45]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[46]  P. Levitt,et al.  A membrane glycoprotein associated with the limbic system mediates the formation of the septo- hippocampal pathway in vitro , 1989, Neuron.

[47]  P. Maclean Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). , 1952, Electroencephalography and clinical neurophysiology.

[48]  C. Gerfen The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. , 1992, Annual review of neuroscience.

[49]  M. Herkenham,et al.  Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum , 1981, Nature.

[50]  André Parent,et al.  Chemical anatomy of primate basal ganglia , 1995, Progress in Neurobiology.

[51]  S. Haber,et al.  Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization. , 1990, Brain research. Developmental brain research.

[52]  P. Levitt,et al.  A monoclonal antibody to limbic system neurons. , 1984, Science.

[53]  G. Paxinos The Rat nervous system , 1985 .

[54]  P. Levitt,et al.  Isolation, biochemical characterization and ultrastructural analysis of the limbic system-associated membrane protein (LAMP), a protein expressed by neurons comprising functional neural circuits , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.