Distribution of Neuronal Melanocortins in the Spadefoot Toad <i>Spea multiplicata</i> and Effects of Stress

Abstract

We examined the effects of an acute stressor on regional alpha-melanocyte-stimulating hormone (αMSH) content in the New Mexican spadefoot toad, Spea multiplicata. We first used immunocytochemistry along with radioimmunoassay (RIA) to examine the distribution of pro-opiomelanocortin (POMC) neurons in the brain of Spea. Neurons immunoreactive for αMSH, β-endorphin, and corticotropin were observed in the preoptic nucleus and ventral infundibulum of the hypothalamus. Ascending immunoreactive fibers projected to the olfactory nucleus, nucleus accumbens, and striatum. Numerous immunoreactive fibers were also observed in the hypothalamus. The thalamus/hypothalamus (T/HT) contained the greatest concentrations of αMSH as determined by RIA followed by the preoptic area (PO). Levels in the telencephalon, brain stem, and optic tectum (OT) were 14–23 times lower than in the T/HT. Exposure to a brief stressor elevated αMSH levels in the PO and OT. We conclude that Spea possesses two distinct POMC neuronal cell groups, one located in the anterior preoptic area and one located in the ventral infundibulum. Ascending projections to the basal ganglia might play an indirect role in tectal regulation and the control of prey-catching behavior. Exposure to an acute stressor alters brain αMSH content in Spea, although there are regional and temporal differences in the response pattern compared to Bufo. These findings are consistent with the notion that neuronal melanocortins influence how frogs and toads gather information about their environment during stress.

Stress, Neuropeptides, and Feeding Behavior: A Comparative Perspective

“…Two major lines of evidence suggest an endogenous role for neuronal melanocortins in regulating feeding behavior in toads. First, melanocortin neurons innervate areas involved in visuomotor processing (Rana ridibunda, Benyamina et al, 1986; Bufo cognatus, Kim and Carr, 1997;Xenopus laevis, Tuinhof et al, 1998; Spea multiplicata, Venkatesan and Carr, 2001). A second line of evidence is work in our lab showing that that brain ␣MSH is altered during and after exposure to a noxious stimulus (Olsen et al, 1999) or confinement (Kim and Carr, 1997).…”

“…Recent anatomical studies support the concept that hypothalamic neuropeptides target sensory and motor circuits involved in simple decision making processes, such as predator/prey recognition. In amphibians and reptiles, melanocortins innervate basal forebrain structures involved in subcortical visuomotor processing, specifically the basal ganglia (Khachaturian et al, 1984;Benyamina et al, 1986;Kim and Carr, 1997;Tuinhof et al, 1998;Venkatesan and Carr, 2001;Fig. 1C).…”

“…1C). In toads, the basal ganglia are innervated by POMC neurons (Kim and Carr, 1997;Venkatesan and Carr, 2001). The striatum (and to a lesser degree the nucleus accumbens) supply both direct and indirect innervation to the optic tectum (Wilczynski and Northcutt, 1983;Marin et al, 1997Marin et al, , 1998.…”

I'll take the low road: the evolutionary underpinnings of visually triggered fear

“…Expression of the receptors and the POMC mRNA is reduced in the SC after transection of the optic nerve (Lindqvist et al, 2003 ). In toads ( Spea multiplicata and Bufo speciosus , detectable levels of N-acetyl ACTH 1-13 amide, or α-melanocyte-stimulating hormone (α-MSH), were found in the OT by radioimmunoassay and immunocytochemistry (Olsen et al, 1999 ; Venkatesan and Carr, 2001 ). Proopiomelanocortin (POMC) -producing cells in the non-mammalian brain are generally limited to one or two hypothalamic areas, depending upon the species, with every species examined to date possessing POMC cells in the ventral infundibular nucleus (presumably homologous to the arcuate POMC cell group in mammals; Venkatesan and Carr, 2001 ).…”

“…Peripheral administration of α-MSH enters the brain (Olsen et al, 1999 ) and accelerates habituation to artificial prey in the Texas toad Bufo speciosus and the Great Plains toad Bufo cognatus (Carpenter and Carr, 1996 ; Olsen et al, 1999 ). Exposure to a non-specific stressor alters the content of α-MSH in the OT (Venkatesan and Carr, 2001 ), suggesting that this peptide may reduce prey-capture when a threat is present.…”