Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: Toward a global 3D model

Abstract

The paraventricular nucleus of the hypothalamus (PVH) coordinates neuroendocrine, autonomic, and behavioral responses to help maintain energy and body water balance. The rat paraventricular nucleus has three major divisions: descending with axonal projections to somatomotor-behavioral and autonomic circuitry, magnocellular neuroendocrine with projections directly to the posterior pituitary, and parvicellular neuroendocrine with projections to the median eminence for controlling anterior pituitary hormone secretion. The present work was undertaken to provide high-resolution mapping of spatial relationships among the two magnocellular neuroendocrine and five parvicellular neuroendocrine neuron types throughout the nucleus. Double immunohistochemical labeling for two neuron types combined with retrograde labeling to identify neuroendocrine neurons positively was used in individual sections spaced 45 mum apart, along with a grid transfer method for reducing plane of section artifacts when comparing staining pattern data between animals. The results indicate that whereas each neuroendocrine neuron phenotype displays a unique distribution pattern, there is extensive partial overlap in a complex pattern between small "hot spots" with a relatively high density of a particular neuron type and few if any other phenotypes. In addition, the distribution of non-neuroendocrine neurons staining with each of the markers (but not retrogradely labeled) was mapped and compared with each other and with the neuroendocrine neuron populations. This spatial organization raises important questions about the differential functional regulation of individual-and perhaps sets of-neuroendocrine motor neuron populations in the PVH by synaptic mechanisms and by less traditional mechanisms like dendritic neurotransmitter release and gap junctions within and between neuron types.

Microdissection of neural networks by conditional reporter expression from a Brainbow herpesvirus

“…The PVN exerts prominent influences over endocrine and autonomic regulation, particularly as it relates to cardiovascular homeostasis and responses to stress (41,42). Retrograde transneuronal passage of virus from peripheral tissues infects PVN neurons in all of the preautonomic subdivisions of this complex cell group, but the precise pathways through which the PVN controls autonomic outflow in an organ-specific fashion are not known.…”

Central Autonomic System

“…It consists of a number of distinct subnuclei, subserving a variety of neuroendocrine and autonomic functions. While much of our information on these subnuclei was originally derived in rats (Swanson and Sawchenko, 1980;Simmons and Swanson, 2009), more recent work has identified comparable complexity in the subnuclear organization of the paraventricular nucleus in mice (Biag et al, 2012). In general, the paraventricular nucleus may be divided into magnocellular and parvicelluar divisions.…”

Organization of the Hypothalamus

“…Accordingly, the paraventricular nucleus is thought to play a central role in mediating hypothalamic responses to stress, feeding, drinking behavior and participates in a variety of autonomic responses (Swanson and Mogenson, 1981;Loewy, 1991;Sawchenko, 1991Sawchenko, , 1998Sawchenko et al, 1996;Elmquist et al, 1999;Geerling et al, 2010). The nucleus is composed of parvicellular and magnocellular divisions, and each division is composed of distinct subdivisions that have characteristic connections and distributions of neurotransmitter specific populations of neurons (Armstrong et al, 1980;Swanson and Kuypers, 1980b;Simmons and Swanson, 2009 ). As a whole, the parvicellular parts of the paraventricular nucleus share strong bi-directional connections with other nuclei in the periventricular zone such as the AVPV and arcuate nucleus (Gu and Simerly 1997;Levin et al, 1987, Li et al, 2000 as well as with the medial part of the medial preoptic nucleus, dorsomedial nucleus and ventral premammillary nucleus (Sawchenko and Swanson 1983b;Swanson 1986, 1988;Thompson et al, 1996).…”