Organization and number of orexinergic neurons in the hypothalamus of two species of Cetartiodactyla: A comparison of giraffe (Giraffa camelopardalis) and harbour porpoise (Phocoena phocoena)

Abstract

The present study describes the organization of the orexinergic (hypocretinergic) neurons in the hypothalamus of the giraffe and harbour porpoise – two members of the mammalian Order Cetartiodactyla which is comprised of the even-toed ungulates and the cetaceans as they share a monophyletic ancestry. Diencephalons from two sub-adult male giraffes and two adult male harbour porpoises were coronally sectioned and immunohistochemically stained for orexin-A. The staining revealed that the orexinergic neurons could be readily divided into two distinct neuronal types based on somal volume, area and length, these being the parvocellular and magnocellular orexin-A immunopositive (OxA+) groups. The magnocellular group could be further subdivided, on topological grounds, into three distinct clusters – a main cluster in the perifornical and lateral hypothalamus, a cluster associated with the zona incerta and a cluster associated with the optic tract. The parvocellular neurons were found in the medial hypothalamus, but could not be subdivided, rather they form a topologically amorphous cluster. The parvocellular cluster appears to be unique to the Cetartiodactyla as these neurons have not been described in other mammals to date, while the magnocellular nuclei appear to be homologous to similar nuclei described in other mammals. The overall size of both the parvocellular and magnocellular neurons (based on somal volume, area and length) were larger in the giraffe than the harbour porpoise, but the harbour porpoise had a higher number of both parvocellular and magnocellular orexinergic neurons than the giraffe despite both having a similar brain mass. The higher number of both parvocellular and magnocellular orexinergic neurons in the harbour porpoise may relate to the unusual sleep mechanisms in the cetaceans.

Orexinergic bouton density is lower in the cerebral cortex of cetaceans compared to artiodactyls

“…As this parvocellular orexinergic cluster had not been previously identified in other species, nor had the differences in neuronal numbers and size been reported, Dell et al (2012) concluded that the orexinergic system is potentially more complex in Cetartiodactyla compared to other mammals; however, it is currently unclear whether these novel findings are associated with differences in the terminal networks of the orexinergic system in these species and if differences do occur, whether they have any functional…”

“…In most mammals the majority of these orexinergic neurons are found within the lateral hypothalamus and perifornical area, but have also been observed in the zona incerta region and the ventrolateral hypothalamus near the optic tract (Peyron et al, 1998;van den Pol, 1999;Wagner et al, 2000;Iqbal et al, 2001;Moore et al, 2001;Yoshida et al, 2006;Nixon and Smale, 2007;Datta and MacLean, 2007;Ettrup et al, 2010;Kruger et al, 2010;Bhagwandin et al, 2011a,b;Gravett et al, 2011;Calvey et al, 2013;Dell et al, 2013;Maseko et al, 2013). A study by Dell et al (2012) comparing the distribution and number of orexinergic neurons in the brain of the giraffe and harbour porpoise showed an additional novel medially located parvocellular cluster of orexinergic neurons in the hypothalamus of these two species, which has since also been reported in the African elephant (Maseko et al, 2013).…”

“…Given these variations in the life histories, environments and behaviour of the members of the Cetartiodactyla order, these species may provide an important model for understanding the role of orexinergic neurons and their terminal networks (Dell et al, 2012). It has been reported that sustained arousal, vigilance and cognitive function may be mediated via orexinergic projections to the cortex (Bayer et al, 2004;Yamada et al, 2008).…”

“…Thus, the density of orexin boutons in the cerebral cortex may provide an indication of the degree to which orexin innervation modulates the activity of cortical neurons to support the behaviours associated with depolarization of hypothalamic orexinergic neurons. Given the higher number of orexinergic neurons in the cetacean hypothalamus compared to the artiodactyl hypothalamus (Dell et al, 2012), it is possible that cetaceans have an increased bouton density in the cerebral cortex; however, this possibility needs to be balanced with the observation that the orexinergic neurons in the artiodactyls are larger than those in cetaceans, and thus may support larger and more branched axons than the cetaceans, leading to a higher orexin bouton density in the artiodactyl cerebral cortex. In order to determine which of these possibilities, if either, occurs, the current study provides a comparison of orexinergic bouton density in the cerebral cortex of a number of Cetartiodactyl species by means of immunohistochemical staining and stereological analysis.…”

Nuclear organisation of some immunohistochemically identifiable neural systems in three Afrotherian species—Potomogale velox, Amblysomus hottentotus and Petrodromus tetradactylus

“…Three exceptions to this organization have been reported in the literature. Both hamsters and microchiropterans appear to lack the optic tract cluster of orexinergic neurons (Mintz et al, 2001;McGranaghan and Piggins, 2001;Korooshi and Klingenspor, 2005;Vidal et al, 2005;Kruger et al, 2010), while the cetartiodactyla, represented by the giraffe and harbour porpoise, are reported to have an additional cluster of parvocellular orexinergic neurons in the medial hypothalamus (Dell et al, 2012). Thus, for the most part, the organization of the orexinergic system is also quite conservative across mammals.…”