Absence of carotid rete mirabile in small tropical ruminants: implications for the evolution of the arterial system in artiodactyls

The intracranial carotid rete (or rete mirabile epidurale) is a unique blood vascular system supplying the brain of artiodactyls, which have either an involuted or no internal carotid artery. Although the lesser and greater mouse deer (Tragulus javanicus and T. napu, respectively) are ruminants, the rete mirabile epidurale is absent. In these animals, as in non-artiodactyls, such as canines, equines and humans, the complete internal carotid artery supplies the brain. It is currently uncertain whether the absence of the rete is confined to mouse deer among ruminants. The absence of the rete in mouse deer provides new insights into the evolution of the arterial system in artiodactyls.     

Selective brain cooling in mammals and birds

Artiodactyls and felids have a carotid rete that can cool the blood destined for the brain and consequently the brain itself if the cavernous sinus receives cool blood returning from the nose. This condition is usually fulfilled in resting and moderately hyperthermic animals. During severe exercise hyperthermia, however, the venous return from the nose bypasses the cavernous sinus so that brain cooling is suppressed. This is irreconcilable with the assumption that the purpose of selective brain cooling (SBC) is to protect the brain from thermal damage. Alternatively, SBC is seen as a mechanism engaging the thermoregulatory system in a water-saving economy mode in which evaporative heat loss is inhibited by the effects of SBC on brain temperature sensors. In nonhuman mammals that do not have a carotid rete, no evidence exists of whole-brain cooling. However, the surface of the cavernous sinus is in close contact with the base of the brain and is the likely source of unregulated regional cooling of the rostral brain stem in some species. In humans, the cortical regions next to the inner surface of the cranium are very likely to receive some regional cooling via the scalp-sinus pathway, and the rostral base of the brain can be cooled by conduction to the nearby respiratory tract; mechanisms capable of cooling the brain as a whole have not been found. Studies using conventional laboratory techniques suggest that SBC exists in birds and is determined by the physical conditions of heat transfer from the head to the environment instead of physiological control mechanisms. Thus except for species possessing a carotid rete, neither a coherent pattern of SBC nor a unifying concept of its biological significance in mammals and birds has evolved.     

Elephants Have Relatively the Largest Cerebellum Size of Mammals

The current study used MR imaging to determine the volume of the cerebellum and its component parts in the brain of three adult male African elephants (Loxodonta africana) and compared this with published data from Asian elephants and other mammalian species including odontocete cetaceans, primates, chiropterans, insectivores, carnivores, and artiodactyls. The cerebellum of the adult elephant has a volume of ～925 mL (average of both African and Asian species). Allometric analysis indicates that the elephant has the largest relative cerebellum size of all mammals studied to date. In addition, both odontocete cetaceans and microchiropterans appear to have large relative cerebellar sizes. The vermal and hemispheric components of the African elephant cerebellum are both large relative to other mammals of similar brain size, however, for odontocete cetaceans the vermal component is small and the hemispheric component is large. These volumetric observations are related to life‐histories and anatomies of the species investigated. The current study provides context for one aspect of the elephant brain in the broader picture of mammalian brain evolution. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.     

A Comparison of the Cortical Structure of the Bowhead Whale (Balaena mysticetus), a Basal Mysticete,with Other Cetaceans

Few studies exist of the bowhead whale brain and virtually nothing is known about its cortical cytoarchitecture or how it compares to other cetaceans. Bowhead whales are one of the least encephalized cetaceans and occupy a basal phylogenetic position among mysticetes. Therefore, the bowhead whale is an important specimen for understanding the evolutionary specializations of cetacean brains. Here, we present an overview of the structure and cytoarchitecture of the bowhead whale cerebral cortex gleaned from Nissl-stained sections and magnetic resonance imaging (MRI) in comparison with other mysticetes and odontocetes. In general, the cytoarchitecture of cetacean cortex is consistent in displaying a thin cortex, a thick, prominent layer I, and absence of a granular layer IV. Cell density, composition, and width of layers III, V, and VI vary among cortical regions, and cetacean cortex is cell-sparse relative to that of terrestrial mammals. Notably, all regions of the bowhead cortex possess high numbers of von Economo neurons and fork neurons, with the highest numbers observed at the apex of gyri. The bowhead whale is also distinctive in having a significantly reduced hippocampus that occupies a space below the corpus callosum within the lateral ventricle. Consistent with other balaenids, bowhead whales possess what appears to be a blunted temporal lobe, which is in contrast to the expansive temporal lobes that characterize most odontocetes. The present report demonstrates that many morphological and cytoarchitectural characteristics are conserved among cetaceans, while other features, such as a reduced temporal lobe, may characterize balaenids among mysticetes. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:745–760, 2019. © 2018 Wiley Periodicals, Inc.     

Naked Mole-Rats: Blind,Naked, and Feeling No Pain

Around the world and across taxa, subterranean mammals show remarkable convergent evolution in morphology (e.g., reduced external ears, small eyes, shortened limbs and tails). This is true of sensory systems as well (e.g., loss of object vision and high frequency hearing). The naked mole-rat (Heterocephalus glaber) displays these typical subterranean features, but also has unusual characteristics even among subterranean mammals. Naked mole-rats are cold-blooded, completely furless, very long-lived (> 30 years), and eusocial (like termites). They also live in large colonies, which is very unusual for subterraneans. Their cortical organization has reduced area for visual processing, utilizing 30% more cortex for tactile processing. They are extremely tolerant to oxygen deprivation, and can recover from 18 min of anoxia. Their pain pathway is reduced and they feel no pain from acidosis. They are the only rodent tested to date whose pheromone-detecting vomeronasal organ shows no postnatal growth. These features may be a result of this species' “extreme subterranean lifestyle” that combines living underground and living in large colonies. Many respiring animals cramped together in unventilated burrows elevates CO₂ levels, high enough to cause acidosis pain, and depletes O₂ concentrations low enough to kill other mammals. The naked mole-rat may be an extreme model of adaptation to subterranean life and provides insights into the complex interplay of evolutionary adaptations to the constraints of subterranean living. Anat Rec, 2018. © 2018 American Association for Anatomy.     

Mysticetes to MiniConference to Manuscripts: Introduction to Thematic Issue on Mysticete Anatomy

This issue of the Anatomical Record is focused on the theme of Mysticete Anatomy. There are six included articles that explore the anatomy of the nasal region (Marquez et al., 2018; Maust-Mohl et al., 2018), larynx (Damien et al., 2018), lungs (Fetherston et al., 2018), sublingual fascia (Werth et al., 2018), and brain (Raghanti et al., 2018). These papers document anatomical features exhibited by mysticetes (baleen whales) and their related cousins (including other whales, and the semiaquatic moose and hippopotamus). This theme stems from a 2-day MiniConference on Mysticete Anatomy, hosted at the Icahn School of Medicine at Mount Sinai in New York City on May 2016. Anatomy is explored in the contexts of function and evolution of aquatic adaptations. Anat Rec, 2019. © 2019 Wiley Periodicals, Inc. Anat Rec, 302:663–666, 2019. © 2019 Wiley Periodicals, Inc.     

Adaptations of the Marsupial Newborn: Birth as an Extreme Environment

At birth a mammalian neonate enters an extreme environment compared to the intrauterine environment in which it has grown. This transition may be particularly extreme in marsupials because they are born at an exceedingly altricial state, after an exceptionally short gestation. Their stage of development must be considered embryonic by almost any criteria. Yet at this very early stage of development marsupials must travel to the teat, attach and suckle, and have basic functioning of all major physiological systems. In this article, we review the adaptations of the marsupial neonate for survival at an embryonic state, showing that the neonate exhibits a mosaic of accelerations and delays of various tissues and organs as well as several special adaptations to produce the functioning newborn. We then discuss the development of the craniofacial region, the body axis and limbs in order to detail some of the major changes to development leading to this uniquely configured neonate. We show that marsupial development arises out of a variety of heterochronies (changes in relative timing of events) and heterotopies (changes in location of specific developmental events) at the genetic, cellular and organ level. We argue that these data support hypotheses that many of the specific patterns seen in marsupial development arise from the basic constraint of embryonic energetic and tissue resources. Finally ideas on the evolutionary context of the marsupial developmental strategy are briefly reviewed. Anat Rec, 2019. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:235–249, 2020. © 2018 American Association for Anatomy     

Tympanic temperature is not suited to indicate selective brain cooling in humans: a re-evaluation of the thermophysiological basics

Selective brain cooling in humans, with venous blood returning from the head surface as the relevant heat sink, was proposed more than two decades ago as a mechanism protecting the brain against damage in hyperthermic conditions. Brain cooling was inferred from decreases of tympanic temperature under the premise that it reflected brain temperature closely, even in conditions of external head cooling. In mammals with a well-developed carotid rete selective brain cooling and its quantitative relevance are experimentally well established by directly monitoring brain temperature. For humans, however, the dispute about the existence and physiological relevance of selective brain cooling has remained unsettled, especially, as far as arguments have been exchanged on the basis of thermophysiological data and model calculations considering brain metabolism, brain hemodynamics and the anatomical preconditions for arterio-venous heat exchange. In this essay two seminal studies in support of the existence of human selective brain cooling in the condition of exercise hyperthermia, with and without dehydration, are re-examined from two points of view: first the stringency of the working hypotheses underlying data evaluation and their subsequent fate. Second the minimum theoretical requirements for data interpretation. The working hypotheses supporting data interpretation in favor of selective brain cooling in humans were heuristic and/or had become questionable at the dates of their application; today, they may be considered as outdated. Data interpretation becomes most conclusive, if tympanic temperature simply is not taken into account.     

The Cerebral Cortex of the Pygmy Hippopotamus,Hexaprotodon liberiensis (Cetartiodactyla,Hippopotamidae): MRI,Cytoarchitecture, and Neuronal Morphology

The structure of the hippopotamus brain is virtually unknown because few studies have examined more than its external morphology. In view of their semiaquatic lifestyle and phylogenetic relatedness to cetaceans, the brain of hippopotamuses represents a unique opportunity for better understanding the selective pressures that have shaped the organization of the brain during the evolutionary process of adaptation to an aquatic environment. Here we examined the histology of the cerebral cortex of the pygmy hippopotamus (Hexaprotodon liberiensis) by means of Nissl, Golgi, and calretinin (CR) immunostaining, and provide a magnetic resonance imaging (MRI) structural and volumetric dataset of the anatomy of its brain. We calculated the corpus callosum area/brain mass ratio (CCA/BM), the gyrencephalic index (GI), the cerebellar quotient (CQ), and the cerebellar index (CI). Results indicate that the cortex of H. liberiensis shares one feature exclusively with cetaceans (the lack of layer IV across the entire cerebral cortex), other features exclusively with artiodactyls (e.g., the morphologiy of CR‐immunoreactive multipolar neurons in deep cortical layers, gyrencephalic index values, hippocampus and cerebellum volumetrics), and others with at least some species of cetartiodactyls (e.g., the presence of a thick layer I, the pattern of distribution of CR‐immunoreactive neurons, the presence of von Economo neurons, clustering of layer II in the occipital cortex). The present study thus provides a comprehensive dataset of the neuroanatomy of H. liberiensis that sets the ground for future comparative studies including the larger Hippopotamus amphibius. Anat Rec, 297:670–700, 2014. © 2014 Wiley Periodicals, Inc.     

Morpho‐Functional Features of the Gonads of Danio rerio: the Role of Brain‐Derived Neurotrophic Factor

Zebrafish, a suitable and widely used teleost fish model in basic biomedical research, displays morphophysiological features of adult gonads that share some commonalities with those of mammalian species. In mammals, gametogenesis is regulated, among several factors, by brain‐derived neurotrophic factor (BDNF). This neurotrophin has a well‐established role in the developing and adult nervous system, as well as gonads development and functions in vertebrate species. We hypothesize that BDNF has a role also in the gonadal functions of zebrafish. At this purpose, we investigated BDNF and its receptors p75 and TrkB in the ovary and testis of adult zebrafish, kept under laboratory conditions. Our results display (1) the expression of BDNF mRNA and pro‐BDNF protein outside of the nervous system, specifically in the ovary and testis; (2) the presence of pro‐BDNF in primary oocytes and follicular layer, and p75 in follicular cells; (3) the localization of pro‐BDNF in type B spermatogonia, and Sertoli cells in testis. Altogether, these data lead us to consider that BDNF is involved in the gonadal function of adult zebrafish, and mainly in the adult ovary. Anat Rec, 2017. © 2017 Wiley Periodicals, Inc. Anat Rec, 301:140–147, 2018. © 2017 Wiley Periodicals, Inc.     

Selective brain cooling in hyperthermia: the mechanisms and medical implications

We hypothesize that selective brain cooling (SBC) can occur in hyperthermic humans despite the fact that humans have no carotid rete, a vascular structure that facilitates countercurrent heat exchange and that is located at the base of the skull in some mammals. We postulate that an increase in emissary and angular ocular venous flows contributes to SBC. The efficiency of SBC is increased by evaporation of sweat on the head and by ventilation through the nose. A body position that increases the intravenous pressure gradient across the skull increases emissary flows and hence enhances the efficiency of SBC. The validity of using tympanic temperature as an index of brain temperature is also postulated.     

Internal Ophthalmic Arteries Within the Brain‐Base Arterial System in Guinea Pig

In situ vascular specimens of the arterial circle were collected from 15 adult guinea pigs, both male and female. After specimen preparation, the vessels were filled with synthetic latex and subjected to analysis. Similar as in the case of other rodents, vertebral arteries were merged into basilar artery, further dividing into two short terminal branches. Distally, the terminal branches extend into caudal cerebral arteries. Rostral part of the arterial circle of brain is supplied with blood from maxillary arteries via external and internal ophthalmic arteries connected by a short anastomosis. This type of vascularity may probably be considered a functional analogy to the internal carotid arteries observed in other species. Rostral and caudal parts of the arterial circle of brain are connected by exceptionally long caudal communicating arteries. In author's opinion, the disputable contribution of internal carotid artery and the exceptional contribution of internal ophthalmic arteries in the cerebral blood supply in guinea pigs as compared to other rodents, warrants further research on the subject. Anat Rec, 301:887–891, 2018. © 2017 Wiley Periodicals, Inc.     

The Eurasian Elk's (Alces alces) Brain Base Arteries in View of Vascular Variation

This article presents the results of analysis of the arterial vascular region of the Eurasian elk, which is a representative of the Cervidae family. The study was conducted on 39 Eurasian elks. The head arteries of 25 animals were filled with LBS 3040 synthetic latex. The head arteries of the other 14 Eurasian elks were filled with an acetone solution of stained chlorinated polyvinyl chloride and macerated. The arterial circle of the Eurasian elk's brain is composed of bilateral rostral cerebral arteries and caudal communicating arteries. The basilar artery closes the arterial circle caudally. The rostral cerebral artery first ramifies into the rostral choroidal artery, then, the middle cerebral artery and the rostral communicating artery. The caudal cerebral artery and the rostral cerebellar artery branch off the caudal communicating artery. The arterial pattern of the Eurasian elk's brain base is similar to the arteries found in other deer. Like in other Ruminantia, the rostral epidural rete mirabile is a unique structure in the Eurasian elk's arterial system. Anat Rec, 302:339–345, 2019. © 2018 Wiley Periodicals, Inc.     

The carotid and orbital retia of the pronghorn,deer and elk

Selective cooling of the brain during heat stress has been shown by others to be a method of temperature regulation for mammals having carotid retia. This study describes the macroscopic anatomy of the cranial circulation of elk, deer and pronghorn as it might pertain to the functioning of carotid retia and orbital retia as heat exchangers. Emphasis has been placed on describing the source of venous blood bathing these retia, for blood flow from these sources to the ophthalmic plexus and cavernous sinus will establish a temperature difference between arterial and venous blood, and influence the magnitude of this gradient. The pronghorn possesses a carotid rete with greater density and smaller calibre vessels overall and a more highly vascular orbital rete compared to the elk and the deer. These anatomical differences may indicate differences in efficiency of heat exchange in the retia. It is suggested that the orbital rete is anatomically in a position to moderate extremes of temperature by cooling arterial blood flowing to neural tissue of the eye and olfactory bulbs.     

Absence of selective brain cooling in free-ranging zebras in their natural habitat

We used implanted miniature data loggers to measure brain and arterial blood temperatures in three free-ranging zebras (Equus burchelli) in their natural habitat, every 5 min for 9 days. The animals experienced globe temperatures exceeding 40 C, and radiant heat load of about 1000 W m-2. Arterial blood exhibited a moderate amplitude (1.7 C) nychthemeral rhythm, with an acrophase at 19.00 h and a nadir late in the morning, at 10.00 h. Brain temperature consistently exceeded blood temperature, on average by 0.2-0.4 C, and changes in brain temperature closely tracked changes in blood temperature. There was no evidence of selective brain cooling, even during the hyperthermia which followed surgery or that associated with intense, short-duration exercise. The relationship between brain and arterial blood temperatures in free-ranging zebras was unlike that reported for horses in the laboratory. Our results do not support the view that mammals lacking a carotid rete can achieve selective brain cooling.     

The Arteries of Brain Base in Species of Bovini Tribe

Studies were conducted on 78 preparations of head and brain arteries in four species of Bos genus, that is in domestic cattle (N = 59), including 22 foetuses (CRL 36.5–78.5 cm), in banteng (Bos javanicus, N = 3), yak (Bos mutus f. grunniens, N = 2), American bison (Bison bison, N = 4), and European bison (Bison bonasus, N = 10). The comparative analysis permitted to demonstrate a similar pattern of brain base arteries in the studied animals. In the studied species, blood vessels of the arterial circle of the brain were found to form by bifurcation of intracranial segments of inner carotid arteries, which protruded from the paired rostral epidural rete mirabile. In Bovidae arterial circle of the brain was supplied with blood mainly by maxillary artery through the blood vessels of the paired rostral epidural rete mirabile. The unpaired caudal epidural rete mirabile was participating in blood supply to the arterial circle of the brain from vertebral and occipital arteries. It manifested character of a taxonomic trait for species of Bos and Bison genera. Basilar artery in all the examined animals manifested a variable diameter, with preliminary portion markedly narrowed, which prevented its participation in blood supply to the arterial circle of the brain. The results and taxonomic position of the species made the authors to suggest a hypothesis that a similar arterial pattern on the brain base might be present also in other species, not included in this analysis. Anat Rec, 296:1677–1682, 2013. © 2013 Wiley Periodicals, Inc.     

Effective Mechanical Advantage Allometry of Felid Elbow and Knee Extensors

Larger terrestrial mammals have generally been found to use more extended limb postures, a mechanism which maintains muscular requirements at larger sizes by improving the effective mechanical advantage (EMA) of limb musculature. Felids, however, have been documented to maintain joint angles across body sizes. If felid morphology scales isometrically, it would mean larger felids have relatively weaker muscles, compromising locomotor activities. Here, we examine the allometric relationships between the EMA of the elbow and knee extensors and body mass, finding that the EMA of the triceps brachii and quadriceps muscles scale with positive allometry. When species-specific joint angles were used rather than felid-average joint angles, EMA scales to body mass with more positive allometry. When the scaling of the muscle and ground reaction force (GRF) lever arms were investigated individually the allometric signal was lost; however, the muscle lever arms generally have allometric slope coefficients that are consistent with positive allometry, while the GRF lever arms demonstrate negative allometric slope coefficients. This suggests there are subtle alterations to limb morphology allowing different felid species to achieve an increased EMA via distinctive mechanisms. The quadriceps EMA was found to scale with sufficient positive allometry to compensate for increases in size without alteration in muscular anatomy; however, this is not the case for the triceps brachii EMA. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:775–784, 2019. © 2018 Wiley Periodicals, Inc.     

Unilateral selective brain cooling

In species with a carotid rete the arterial blood flowing to the brain can be cooled by passing the carotid rete. The mechanism is termed selective brain cooling (SBC). The aim of the study was to evaluate whether SBC could be induced unilaterally. 27 experiments were performed in 2 conscious goats which were prepared with carotid loops to manipulate the blood temperature of the left and right carotid artery independently of each other. The temperature of the left and right hemisphere of the brain was controlled by means of extracorporeal heat exchangers acting on the carotid blood while trunk temperature was clamped at 39.5 °C by a heat exchanger in an arteriovenous shunt. Unilateral warming of the brain induced ipsilateral SBC only, and was accompanied by a bilateral increase of the ear skin temperature. The results demonstrate the precise control of brain temperature by SBC since even unilateral temperature deviations of the brain can be reduced by SBC. In conclusion SBC regulates the temperature of single hemispheres rather than the mean brain temperature.     

Vascular Patterns in the Heads of Dinosaurs: Evidence for Blood Vessels,Sites of Thermal Exchange,and Their Role in Physiological Thermoregulatory Strategies

Body size has thermal repercussions that impact physiology. Large-bodied dinosaurs potentially retained heat to the point of reaching dangerous levels, whereas small dinosaurs shed heat relatively easily. Elevated body temperatures are known to have an adverse influence on neurosensory tissues and require physiological mechanisms for selective brain and eye temperature regulation. Vascular osteological correlates in fossil dinosaur skulls from multiple clades representing different body-size classes were identified and compared. Neurovascular canals were identified that differentiate thermoregulatory strategies involving three sites of evaporative cooling that are known in extant diapsids to function in selective brain temperature regulation. Small dinosaurs showed similarly sized canals, reflecting a plesiomorphic balanced pattern of blood supply and a distributed thermoregulatory strategy with little evidence of enhancement of any sites of thermal exchange. Large dinosaurs, however, showed a more unbalanced vascular pattern whereby certain sites of thermal exchange were emphasized for enhanced blood flow, reflecting a more focused thermal strategy. A quantitative, statistical analysis of canal cross-sectional area was conducted to test these anatomical results, confirming that large-bodied, and often large-headed, species showed focused thermal strategies with enhanced collateral blood flow to certain sites of heat exchange. Large theropods showed evidence for a plesiomorphic balanced blood flow pattern, yet evidence for vascularization of the large antorbital paranasal air sinus indicates theropods may have had a fourth site of heat exchange as part of a novel focused thermoregulatory strategy. Evidence presented here for differing thermoregulatory strategies based on size and phylogeny helps refine our knowledge of dinosaur physiology. Anat Rec, 303:1075–1103, 2020. © 2019 American Association for Anatomy