Abstract
We examined the postnatal ontogeny of the striatum in rhesus monkeys (Macaca mulatta) to identify temporal and spatial patterns of histological and chemical maturation. Our goal was to determine whether this forebrain structure is developmentally static or dynamic in postnatal life. Brains from monkeys at 1 day, 1, 4, 6, 9, and 12 months of age (N = 12) and adult monkeys (N = 4) were analyzed. Nissl staining was used to assess striatal volume, cytoarchitecture, and apoptosis. Immunohistochemistry was used to localize and measure substance P (SP), leucine-enkephalin (LENK), tyrosine hydroxylase (TH), and calbindin D28 (CAL) immunoreactivities. Mature brain to body weight ratio was achieved at 4 months of age, and striatal volume increased from ∼1.2 to ∼1.4 cm3 during the first postnatal year. Nissl staining identified, prominently in the caudate nucleus, developmentally persistent discrete cell islands with neuronal densities greater than the surrounding striatal parenchyma (matrix). Losses in neuronal density were observed in island and matrix regions during maturation, and differential developmental programmed cell death was observed in islands and matrix regions. Immunohistochemistry revealed striking changes occurring postnatally in striatal chemical neuroanatomy. At birth, the immature dopaminergic nigrostriatal innervation was characterized by islands enriched in TH-immunoreactive puncta (putative terminals) in the neuropil; TH-enriched islands aligned completely with areas enriched in SP immunoreactivity but low in LENK immunoreactivity. These areas enriched in SP immunoreactivity but low in LENK immunoreactivity were identified as striosome and matrix areas, respectively, because CAL immunoreactivity clearly delineated these territories. SP, LENK, and CAL immunoreactivities appeared as positive neuronal cell bodies, processes, and puncta. The matrix compartment at birth contained relatively low TH-immunoreactive processes and few SP-positive neurons but was densely populated with LENK-immunoreactive neurons. The nucleus accumbens part of the ventral striatum also showed prominent differences in SP, LENK, and CAL immunoreactivities in shell and core territories. During 12 months of postnatal maturation salient changes occurred in neurotransmitter marker localization: TH-positive afferents densely innervated the matrix to exceed levels of immunoreactivity in the striosomes; SP immunoreactivity levels increased in the matrix; and LENK-immunoreactivity levels decreased in the matrix and increased in the striosomes. At 12 months of age, striatal chemoarchitecture was similar qualitatively to adult patterns, but quantitatively different in LENK and SP in caudate, putamen, and nucleus accumbens. This study shows for the first time that the rhesus monkey striatum requires more than 12 months after birth to develop an adult-like pattern of chemical neuroanatomy and that principal neurons within striosomes and matrix have different developmental programs for neuropeptide expression. We conclude that postnatal maturation of the striatal mosaic in primates is not static but, rather, is a protracted and dynamic process that requires many synchronous and compartment-selective changes in afferent innervation and in the expression of genes that regulate neuronal phenotypes.
Highlights
The striatum is a subcortical forebrain gray matter com- spiny neurons) but diverse connections and neurotransmitters partment of the basal ganglia comprised of neurons with (Crittenden and Graybiel, 2011; Haber et al, 2012)
Because monkeys that experienced social/sensory deprivation have neurochemical alterations in their basal ganglia (Martin et al, 1991b), and because the behavioral disabilities induced by social/sensory deprivation of infants primates persist into adulthood (Vicedo, 2009) and suggest dysfunction of the basal ganglia, we have hypothesized that the normal postnatal development of the structural and functional organization of the basal ganglia, the dorsal striatum, is partly determined by social environment and experience (Martin et al, 1991b)
Several gradual developmental events were observed in the maturing striatum, including reductions in cellular density, increased innervation by dopaminergic afferents, an initial high expression of LENK followed by a subsequent down-regulation of ENK expression, and a progressive increase in substance P (SP) expression
Summary
The striatum is a subcortical forebrain gray matter com- spiny neurons) but diverse connections and neurotransmitters partment of the basal ganglia comprised of neurons with (Crittenden and Graybiel, 2011; Haber et al, 2012). Anatomical principles of organization of the striatum include the differentiation of the dorsal striatum into at least two primary compartments designated as striosomes (patches) and extrastriosomal matrix (Crittenden and Graybiel, 2011), the differentiation of the nucleus accumbens into core and shell regions (Heimer et al, 1997), and the serial and parallel arrangements of input-output connectivity (Alexander et al, 1986; Heimer and Van Hoesen, 2006; Haber et al, 2012). The normal compartmental arrangements of peptidergic neurotransmitters of striatal output neurons, the localization of neuropeptides within striatal synaptic targets (globus pallidus and substantia nigra), and the dopaminergic afferents to the striatum from substantia nigra are all profoundly altered in adult rhesus monkeys that experienced severe sensory/social deprivation during their first year of infancy (Martin et al, 1991b). This study was initiated to evaluate the temporal and spatial development of striatal cytology and chemical neuroanatomy in normal socially reared infant rhesus monkeys
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
