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Journal of Neuroscience, Vol 11, 3344-3358, Copyright © 1991 by Society for Neuroscience
Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions
LJ Martin, DM Spicer, MH Lewis, JP Gluck and LC Cork
Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205.
Rhesus monkeys (Macaca mulatta) reared during the first year of life
without social contact develop persistent stereotyped movements, self-
directed behaviors, and psychosocial abnormalities, but neurobiological
mechanisms underlying the behaviors of socially deprived (SD) monkeys are
unknown. Monkeys were reared in total social deprivation for the first 9
months of life; control monkeys were reared socially (SR) with mothers and
peers. Subjects were killed at 19-24 yr of age. Because the behaviors of SD
monkeys are reminiscent of changes in striatal or amygdalar function, we
used immunocytochemistry for substance P (SP), leucine-enkephalin (LENK),
somatostatin, calbindin, and tyrosine hydroxylase (TH) to evaluate
qualitatively and quantitatively patterns of neurotransmitter marker
immunoreactivity within subcortical regions. In SD monkeys, the
chemoarchitecture of the striatum was altered. Neuronal cell bodies and
processes immunoreactive for SP and LENK were depleted markedly in patch
(striosome) and matrix regions of the caudate nucleus and putamen; the
average density of SP-immunoreactive neurons was reduced 58% relative to SR
monkeys. Calbindin and TH immunoreactivities were diminished in the matrix
of caudate and putamen of SD monkeys. TH-immunoreactive neurons, but not
cresyl violet-stained neurons, in the substantia nigra pars compacta were
decreased (43%) in SD monkeys. Peptide-immunoreactive terminals were
reduced in the globus pallidus and substantia nigra in SD monkeys. The
nucleus accumbens was the least affected of striatal regions. Striatal
somatostatin immunoreactivity wa qualitatively and quantitatively similar
in SD and SR monkeys. Several regions, for example, bed nucleus of the
stria terminalis, amygdala, and basal forebrain magnocellular complex, that
were in the same sections and are enriched in these markers did not appear
altered in SD monkeys, suggesting a regional specificity for vulnerability.
The altered chemoarchitecture of some basal ganglia regions in adult
monkeys that experienced social deprivation as infants suggests that the
postnatal maturation of neurotransmitter phenotypes in some structures is
influenced by social environment. Abnormal motor and psychosocial behaviors
resulting from this form of social/sensory deprivation may result from
alterations in peptidergic and dopaminergic systems within the basal
ganglia.
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