Architectural Organization of the African Elephant Diencephalon and Brainstem

Abstract

The current study examined the organization of the diencephalon and brainstem of the African elephant (Loxodonta africana) - a region of the elephant brain that has not been examined for at least 50 years. The current description, employing material amenable for use with modern neuroanatomical methods, shows that, for the most part, the elephant diencephalon and brainstem are what could be considered typically mammalian, with subtle differences in proportions and topology. The variations from these previous descriptions, where they occurred, were related to four specific aspects of neural information processing: (1) the motor systems, (2) the auditory and vocalization systems, (3) the orexinergic satiety/wakefulness centre of the hypothalamus and the locus coeruleus, and (4) the potential neurogenic lining of the brainstem. For the motor systems, three specific structures exhibited interesting differences in organization - the pars compacta of the substantia nigra, the facial motor nerve nucleus, and the inferior olivary nuclear complex, all related to the timing and learning of movements and likely related to the control of the trunk. The dopaminergic neurons of the substantia nigra appear to form distinct islands separated from each other by large fibre pathways, an appearance unique to the elephant. Each island may send topologically organized projections to the striatum forming a dopaminergic innervation mosaic that may relate to trunk movements. At least five regions of the combined vocalization production and auditory/seismic reception system were specialized, including the large and distinct nucleus ellipticus of the periaqueductal grey matter, the enlarged lateral superior olivary nucleus, the novel transverse infrageniculate nucleus of the dorsal thalamus, the enlarged dorsal column nuclei and the ventral posterior inferior nucleus of the dorsal thalamus. These specializations, related to production and reception of infrasound, allow the proposal of a novel concept regarding the reception and localization of infrasonic sources. The orexinergic system of the hypothalamus displayed a medial hypothalamic parvocellular cluster of neurons in addition to the magnocellular clusters typical of mammals located in the lateral hypothalamus, and a novel medial division of the locus coeruleus was observed in the pons. These systems are related to appetitive drive and promotion of wakefulness, two aspects of elephant behaviour that appear to be inextricably linked. Lastly, we observed an extensive potential neurogenic lining of the ventricles throughout the brainstem that is present in even quite old elephants, although the function of these cells remains elusive. These observations combined demonstrate that, while much of the elephant brainstem is typically mammalian, certain aspects of the anatomy related to specialized behaviour of elephants are present and instructive in understanding elephant behaviour.

The elephant brain in numbers

“…The highly sensitive tip of the trunk moves extensively as the elephant explores and manipulates its immediate environment. We speculate that the extraordinary number of neurons in the elephant cerebellum, and thus the large absolute and relative size of this structure (Maseko et al, 2012) as well as brainstem motor specializations (Maseko et al, 2013b), may have been driven by the processing of complex sensory and motor information regarding the trunk, a large sensorimotor unpaired appendage unique to the Proboscideans.…”

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

“…For example, the orexinergic cells within the hypothalamus can generally be divided into three magnocellular clusters, the main cluster, the zona incerta cluster and the optic tract cluster, although variations do exist (Kruger et al, 2010;Bhagwandin et al, 2011a,b;Gravett et al, 2011;Dell et al, 2012Dell et al, , 2013Calvey et al, 2013;Maseko et al, 2013;Patzke et al, 2014). One of the interesting variations found was the existence of a parvocellular medially located cluster of orexinergic neurons in the giraffe and harbour porpoise (Dell et al, 2012), which has since been reported in the African elephant (Maseko et al, 2013). Thus, the Cetartiodactyla as a group have an additional orexinergic nucleus normally not observed in other mammals.…”

“…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).…”

The Evolutions of Large Brain Size in Mammals: The ‘Over-700-Gram Club Quartet'

“…Recent studies are beginning to demonstrate that the elephant brain, in overall appearance is, unsurprisingly, a typical, but large, mammalian brain; however, it does possess specializations associated with the auditory and vocalization systems [Cozzi et al, 2001;Maseko et al, 2013b], with the portion of the motor system related to the timing of movements [Maseko et al, 2012[Maseko et al, , 2013a, the presence of von Economo neurons [Hakeem et al, 2009], and a very large, both in relative and absolute terms, cerebellum [Maseko et al, 2012[Maseko et al, , 2013a. In addition, it is evident that the morphological complexity of some of the pyramidal neurons in the frontal cortex rivals those seen in human frontal cortex .…”