Leigh-Anne Dell

Nuclear organization of cholinergic, putative catecholaminergic and serotonergic systems in the brains of five microchiropteran species.

The current study describes, using immunohistochemical methods, the nuclear organization of the cholinergic, catecholaminergic and serotonergic systems within the brains of five microchiropteran species. For the vast majority of nuclei observed, direct homologies are evident in other mammalian species; however, there were several distinctions in the presence or absence of specific nuclei that provide important clues regarding the use of the brain in the analysis of chiropteran phylogenetic affinities. Within the five species studied, three specific differences (presence of a parabigeminal nucleus, dorsal caudal nucleus of the ventral tegmental area and the absence of the substantia nigra ventral) found in two species from two different families (Cardioderma cor; Megadermatidae, and Coleura afra; Emballonuridae), illustrates the diversity of microchiropteran phylogeny and the usefulness of brain characters in phylogenetic reconstruction. A number of distinct differences separate the microchiropterans from the megachiropterans, supporting the diphyletic hypothesis of chiropteran phylogenetic origins. These differences phylogenetically align the microchiropterans with the heterogenous grouping of insectivores, in contrast to the alignment of megachiropterans with primates. The consistency of the changes and stasis of neural characters with mammalian phylogeny indicate that the investigation of the microchiropterans as a sister group to one of the five orders of insectivores to be a potentially fruitful area of future research.

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).

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.

Cellular location and major terminal networks of the orexinergic system in the brains of five microchiropteran species.

The present study describes the distribution of Orexin-A immunoreactive cell bodies and terminal networks in the brains of five microchiropteran species. Given the specialized flight and echolocation abilities of the microchiropterans it was of interest to examine if any specific differences in a generally phylogenetically homogenous neural system could be found. The orexinergic neurons have been found within the hypothalamus of all species studied, and were represented by a large cluster that spanned the anterior, dorsomedial, perifornical and lateral hypothalamic regions, with a smaller cluster extending into the region of the medial zona incerta. Evidence for orexinergic neurons in the ventrolateral hypothalamus adjacent to the optic tract was not observed in any microchiropteran species. The terminal networks of the orexinergic neurons conformed to that previously reported in a range of mammalian species, with dense terminal networks being found in the hypothalamus, cholinergic pedunculopontine and laterodorsal tegemental nuclei, the noradrenergic locus coeruleus complex, all serotonergic nuclei, the paraventricular nuclei of the epithalamus and adjacent to the habenular nuclei. Thus, apart from the lack of neurons in the ventrolateral hypothalamus, the orexinergic system of the microchiropterans appears typically mammalian.

Organization of the sleep-related neural systems in the brain of the harbour porpoise (Phocoena phocoena)

The present study provides the first systematic immunohistochemical neuroanatomical investigation of the systems involved in the control and regulation of sleep in an odontocete cetacean, the harbor porpoise (Phocoena phocoena). The odontocete cetaceans show an unusual form of mammalian sleep, with unihemispheric slow waves, suppressed REM sleep, and continuous bodily movement. All the neural elements involved in sleep regulation and control found in bihemispheric sleeping mammals were present in the harbor porpoise, with no specific nuclei being absent, and no novel nuclei being present. This qualitative similarity of nuclear organization relates to the cholinergic, noradrenergic, serotonergic, and orexinergic systems and is extended to the γ‐aminobutyric acid (GABA)ergic elements involved with these nuclei. Quantitative analysis of the cholinergic and noradrenergic nuclei of the pontine region revealed that in comparison with other mammals, the numbers of pontine cholinergic (126,776) and noradrenergic (122,878) neurons are markedly higher than in other large‐brained bihemispheric sleeping mammals. The diminutive telencephalic commissures (anterior commissure, corpus callosum, and hippocampal commissure) along with an enlarged posterior commissure and supernumerary pontine cholinergic and noradrenergic neurons indicate that the control of unihemispheric slow‐wave sleep is likely to be a function of interpontine competition, facilitated through the posterior commissure, in response to unilateral telencephalic input related to the drive for sleep. In addition, an expanded peripheral division of the dorsal raphe nuclear complex appears likely to play a role in the suppression of REM sleep in odontocete cetaceans. Thus, the current study provides several clues to the understanding of the neural control of the unusual sleep phenomenology present in odontocete cetaceans. J. Comp. Neurol. 524:1999–2017, 2016.

Cellular location and major terminal networks of the orexinergic system in the brain of two megachiropterans

The present study describes the distribution of orexin-A immunoreactive neurons and their terminal networks in the brains of two species of megachiropterans. In general the organization of the orexinergic system in the mammalian brain is conserved across species, but as one of two groups of mammals that fly and have a high metabolic rate, it was of interest to determine whether there were any specific differences in the organization of this system in the megachiropterans. Orexinergic neurons were limited in distribution to the hypothalamus, and formed three distinct clusters, or nuclei, a main cluster with a perifornical location, a zona incerta cluster in the dorsolateral hypothalamus and an optic tract cluster in the ventrolateral hypothalamus. The nuclear parcellation of the orexinergic system in the megachiropterans is similar to that seen in many mammals, but differs from the microchiropterans where the optic tract cluster is absent. The terminal networks of the orexinergic neurons in the megachiropterans was similar to that seen in a range of mammalian species, with significant terminal networks being found in the hypothalamus, cholinergic pedunculopontine and laterodorsal tegemental nuclei, the noradrenergic locus coeruleus complex, all serotonergic nuclei, the paraventricular nuclei of the epithalamus and adjacent to the habenular nuclei. While the megachiropteran orexinergic system is typically mammalian in form, it does differ from that reported for microchiropterans, and thus provides an additional neural character arguing for independent evolution of these two chiropteran suborders.

Organization of the sleep-related neural systems in the brain of the river hippopotamus (Hippopotamus amphibius): A most unusual cetartiodactyl species

This study provides the first systematic analysis of the nuclear organization of the neural systems related to sleep and wake in the basal forebrain, diencephalon, midbrain, and pons of the river hippopotamus, one of the closest extant terrestrial relatives of the cetaceans. All nuclei involved in sleep regulation and control found in other mammals, including cetaceans, were present in the river hippopotamus, with no specific nuclei being absent, but novel features of the cholinergic system, including novel nuclei, were present. This qualitative similarity relates to the cholinergic, noradrenergic, serotonergic, and orexinergic systems and is extended to the γ‐aminobutyric acid (GABA)ergic elements of these nuclei. Quantitative analysis reveals that the numbers of pontine cholinergic (259,578) and noradrenergic (127,752) neurons, and hypothalamic orexinergic neurons (68,398) are markedly higher than in other large‐brained mammals. These features, along with novel cholinergic nuclei in the intralaminar nuclei of the dorsal thalamus and the ventral tegmental area of the midbrain, as well as a major expansion of the hypothalamic cholinergic nuclei and a large laterodorsal tegmental nucleus of the pons that has both parvocellular and magnocellular cholinergic neurons, indicates an unusual sleep phenomenology for the hippopotamus. Our observations indicate that the hippopotamus is likely to be a bihemispheric sleeper that expresses REM sleep. The novel features of the cholinergic system suggest the presence of an undescribed sleep state in the hippopotamus, as well as the possibility that this animal could, more rapidly than other mammals, switch cortical electroencephalographic activity from one state to another. J. Comp. Neurol. 524:2036–2058, 2016.

Organization of the sleep-related neural systems in the brain of the minke whale (Balaenoptera acutorostrata)

The current study analyzed the nuclear organization of the neural systems related to the control and regulation of sleep and wake in the basal forebrain, diencephalon, midbrain, and pons of the minke whale, a mysticete cetacean. While odontocete cetaceans sleep in an unusual manner, with unihemispheric slow wave sleep (USWS) and suppressed REM sleep, it is unclear whether the mysticete whales show a similar sleep pattern. Previously, we detailed a range of features in the odontocete brain that appear to be related to odontocete‐type sleep, and here present our analysis of these features in the minke whale brain. All neural elements involved in sleep regulation and control found in bihemispheric sleeping mammals and the harbor porpoise were present in the minke whale, with no specific nuclei being absent, and no novel nuclei being present. This qualitative similarity relates to the cholinergic, noradrenergic, serotonergic and orexinergic systems, and the GABAergic elements of these nuclei. Quantitative analysis revealed that the numbers of pontine cholinergic (274,242) and noradrenergic (203,686) neurons, and hypothalamic orexinergic neurons (277,604), are markedly higher than other large‐brained bihemispheric sleeping mammals. Small telencephalic commissures (anterior, corpus callosum, and hippocampal), an enlarged posterior commissure, supernumerary pontine cholinergic and noradrenergic cells, and an enlarged peripheral division of the dorsal raphe nuclear complex of the minke whale, all indicate that the suite of neural characteristics thought to be involved in the control of USWS and the suppression of REM in the odontocete cetaceans are present in the minke whale. J. Comp. Neurol. 524:2018–2035, 2016.

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

The species of the cetacean and artiodactyl suborders, which constitute the order Cetartiodactyla, exhibit very different sleep phenomenology, with artiodactyls showing typical bihemispheric slow wave and REM sleep, while cetaceans show unihemispheric slow wave sleep and appear to lack REM sleep. The aim of this study was to determine whether cetaceans and artiodactyls have differently organized orexinergic arousal systems by examining the density of orexinergic innervation to the cerebral cortex, as this projection will be involved in various aspects of cortical arousal. This study provides a comparison of orexinergic bouton density in the cerebral cortex of twelve Cetartiodactyla species (ten artiodactyls and two cetaceans) by means of immunohistochemical staining and stereological analysis. It was found that the morphology of the axonal projections of the orexinergic system to the cerebral cortex was similar across all species, as the presence, size and proportion of large and small orexinergic boutons were similar. Despite this, orexinergic bouton density was lower in the cerebral cortex of the cetaceans studied compared to the artiodactyls studied, even when corrected for brain mass, neuron density, glial density and glial:neuron ratio. Results from correlational and principal component analyses indicate that glial density is a major determinant of the observed differences between artiodactyl and cetacean cortical orexinergic bouton density.

The Continuously Growing Central Nervous System of the Nile Crocodile (Crocodylus niloticus)

It is a central assumption that larger bodies require larger brains, across species but also possibly within species with continuous growth throughout the lifetime, such as the crocodile. The current study investigates the relationships between body growth (length and mass) and the rates of growth of various subdivisions of the central nervous system (CNS) (brain, spinal cord, eyes) in Nile crocodiles weighing between 90 g and 90 kg. Although the brain appears to grow in two phases in relation to body mass, initially very rapidly then very slowly, it turns out that brain mass increases continuously as a power function of body mass with a small exponent of 0.256, such that a 10‐fold increase in body mass is accompanied by a 1.8‐fold in brain mass. Eye volume increases slowly with increasing body mass, as a power function of the latter with an exponent of 0.37. The spinal cord, however, grows more rapidly in mass, accompanying body mass raised to an exponent of 0.54, and increasing in length as predicted, with body mass raised to an exponent of 0.32 (close to the predicted 1/3). While supporting the expectation formulated by Jerison that larger bodies require larger brains to operate them, our findings show that: (1) the rate of increase in brain size is very small compared to body growth; and (2) different parts of the CNS grow at different rates accompanying continuous body growth, with a faster increase in spinal cord mass and eye volume, than in brain mass. Anat Rec, 296:1489–1500, 2013.

Hands of living San resemble those in palaeolithic stencils, not modern Europeans

The hand metrics of Palaeolithic artists show a number of distinctive features that contrast with the low-variance hand metrics of modern Europeans, and with the majority of other modern humans. For example, the D2/D4 ratio in the Palaeolithic artists has a much greater spread of values and a greater degree of sexual dimorphism. We find that living San people, who represent the minority of modern humans that have high-variance genetics, also have a hand metric phenotype like the Palaeolithic artists, different from modern Europeans and other low-variance genetics modern humans. The increased variance and sexual dimorphism of the phenotypic D2/D4 ratio in the San measurements are in keeping with genetic evidence that the San represent one of the oldest human lineages with the greatest genetic diversity. The findings have the implication that the European Palaeolithic cave artists may have been derived from San-like migrants who brought an established artistic tradition from Africa to Europe, only to be replaced as a population, leaving no evidence of their genetics in modern Europeans, as observed for other Palaeolithic genes such as Oase 1.