Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions

Abstract

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.

Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents

“…[32]). Similarly, isolation-rearing induces both stereotypy and changes in basal ganglia dopaminergic tone [36,37,42], as does premature weaning [24,63]. Basal ganglia lesions in humans are similarly associated with stereotypy-like behaviour [1,39].…”

Social Isolation in the Rat Produces Developmentally Specific Deficits in Prepulse Inhibition of the Acoustic Startle Response Without Disrupting Latent Inhibition

“…Both isolation-reared animals (those isolated from the weaning age) and isolation-housed animals (those isolated as adults) were hyperactive when placed in a novel environment. Social isolation also led to deficits in PPI of the acoustic startle KEY WORDS: Social isolation; Locomotor activity; Prepulse inhibition; Latent inhibition; Dopamine; Ventral striatumVariations in early social experience have been shown to have profound effects on the adult behavior, brain morphology, and neurochemistry of a variety of spe cies (Sachser 1986;Lewis et al 1990;Martin et al 1991;Jones et al 1992). For example, rearing rats in social iso lation from the weaning age produces behavioral ab normalities that include increases in spontaneous and response that were specific to isolation-reared animals.…”

“…Variations in early social experience have been shown to have profound effects on the adult behavior, brain morphology, and neurochemistry of a variety of spe cies (Sachser 1986;Lewis et al 1990;Martin et al 1991;Jones et al 1992). For example, rearing rats in social iso lation from the weaning age produces behavioral ab normalities that include increases in spontaneous and response that were specific to isolation-reared animals.…”

Is homosexual behaviour hard-wired? Sexual orientation and brain structure

“…Any aetiological explanation of homosexual behaviour based on neuroanatomy would ultimately have to explain how such psychosocial factors exert their effects (see also Baron, 1993). (3) Homosexual thoughts and/or behaviour lead to chemical and structural changes in the brain in the same way as many forms of experience, such as social deprivation and environmental complexity (Walsh, 1981;Martin et al 1991). For example, the promiscuous behaviour and associated lifestyle likely to have been common among homosexual men who die of AIDS may cause selective shrinkage of a subset of hypothalamic neurons or increase the calibre of anterior commissural fibres.…”