Coevolution of motor cortex and behavioral specializations associated with flight and echolocation in bats.

Bats have evolved behavioral specializations that are unique among mammals, including self-propelled flight and echolocation. However, areas of motor cortex that are critical in the generation and fine control of these unique behaviors have never been fully characterized in any bat species, despite the fact that bats compose ∼25% of extant mammalian species. Using intracortical microstimulation, we examined the organization of motor cortex in Egyptian fruit bats (Rousettus aegyptiacus), a species that has evolved a novel form of tongue-based echolocation.1,2 We found that movement representations include an enlarged tongue region containing discrete subregions devoted to generating distinct tongue movement types, consistent with their behavioral specialization generating active sonar using tongue clicks. This magnification of the tongue in motor cortex is comparable to the enlargement of somatosensory representations in species with sensory specializations.3-5 We also found a novel degree of coactivation between the forelimbs and hindlimbs, both of which are involved in altering the shape and tension of wing membranes during flight. Together, these findings suggest that the organization of motor cortex has coevolved with peripheral morphology in bats to support the unique motor demands of flight and echolocation.

The Tempo of Mammalian Embryogenesis: Variation in the Pace of Brain and Body Development.

Why do some species develop rapidly, while others develop slowly? Mammals are highly variable in the pace of growth and development over every stage of ontogeny, and this basic variable - the pace of ontogeny - is strongly associated with a wide range of phenotypes in adults, including allometric patterns of brain and body size, as well as the pace of neurodevelopment. This analysis describes variation in the pace of embryonic development in eutherian mammals, drawing on a collected dataset of embryogenesis in fifteen species representing rodents, carnivores, ungulates, and primates. Mammals vary in the pace of every stage of embryogenesis, including stages of early zygote differentiation, blastulation and implantation, gastrulation, neurulation, somitogenesis, and later stages of basic limb, facial, and brain development. This comparative review focuses on the general variation of rapid vs. slow mammalian embryogenesis, with a focus on the pace of somite formation, brain vs. somatic development, and how embryonic pacing predicts later features of ontogeny.

Distributed Motor Control of Limb Movements in Rat Motor and Somatosensory Cortex: The Sensorimotor Amalgam Revisited.

Which areas of the neocortex are involved in the control of movement, and how is motor cortex organized across species? Recent studies using long-train intracortical microstimulation demonstrate that in addition to M1, movements can be elicited from somatosensory regions in multiple species. In the rat, M1 hindlimb and forelimb movement representations have long been thought to overlap with somatosensory representations of the hindlimb and forelimb in S1, forming a partial sensorimotor amalgam. Here we use long-train intracortical microstimulation to characterize the movements elicited across frontal and parietal cortex. We found that movements of the hindlimb, forelimb, and face can be elicited from both M1 and histologically defined S1 and that representations of limb movement types are different in these two areas. Stimulation of S1 generates retraction of the contralateral forelimb, while stimulation of M1 evokes forelimb elevation movements that are often bilateral, including a rostral region of digit grasping. Hindlimb movement representations include distinct regions of hip flexion and hindlimb retraction evoked from S1 and hip extension evoked from M1. Our data indicate that both S1 and M1 are involved in the generation of movement types exhibited during natural behavior. We draw on these results to reconsider how sensorimotor cortex evolved.

Not all cortical expansions are the same: the coevolution of the neocortex and the dorsal thalamus in mammals.

A central question in comparative neurobiology concerns how evolution has produced brains with expanded neocortices, composed of more areas with unique connectivity and functional properties. Some mammalian lineages, such as primates, exhibit exceptionally large cortices relative to the amount of sensory inputs from the dorsal thalamus, and this expansion is associated with a larger number of distinct cortical areas, composing a larger proportion of the cortical sheet. We propose a link between the organization of the neocortex and its expansion relative to the size of the dorsal thalamus, based on a combination of work in comparative neuroanatomy and experimental research.

Minimal variation in eutherian brain growth rates during fetal neurogenesis.

A central question in the evolution of brain development is whether species differ in rates of brain growth during fetal neurogenesis. Studies of neonatal data have found allometric evidence for brain growth rate differences according to physiological variables such as relative metabolism and placental invasiveness, but these findings have not been tested against fetal data directly. Here, we measure rates of exponential brain growth acceleration in 10 eutherian mammals, two marsupials, and two birds. Eutherian brain acceleration exhibits minimal variation relative to body and visceral organ growth, varies independently of correlated growth patterns in other organs, and is unrelated to proposed physiological constraints such as metabolic rate or placental invasiveness. Brain growth rates in two birds overlap with eutherian variation, while marsupial brain growth is exceptionally slow. Peak brain growth velocity is linked in time with forebrain myelination and eye opening, reliably separates altricial species born before it from precocial species born afterwards, and is an excellent predictor of adult brain size (r2 = 0.98). Species with faster body growth exhibit larger relative brain size in early ontogeny, while brain growth is unrelated to allometric measures. These findings indicate a surprising conservation of brain growth rates during fetal neurogenesis in eutherian mammals, clarify sources of variation in neonatal brain size, and suggest that slow body growth rates cause species to be more encephalized at birth.

Prenatal Brain-Body Allometry in Mammals.

Variation in relative brain size among adult mammals is produced by different patterns of brain and body growth across ontogeny. Fetal development plays a central role in generating this diversity, and aspects of prenatal physiology such as maternal relative metabolic rate, altriciality, and placental morphology have been proposed to explain allometric differences in neonates and adults. Primates are also uniquely encephalized across fetal development, but it remains unclear when this pattern emerges during development and whether it is common to all primate radiations. To reexamine these questions across a wider range of mammalian radiations, data on the primarily fetal rapid growth phase (RGP) of ontogenetic brain-body allometry was compiled for diverse primate (np = 12) and nonprimate (nnp = 16) mammalian species, and was complemented by later ontogenetic data in 16 additional species (np = 9; nnp = 7) as well as neonatal proportions in a much larger sample (np = 38; nnp = 83). Relative BMR, litter size, altriciality, and placental morphology fail to predict RGP slopes as would be expected if physiological and life history variables constrained fetal brain growth, but are associated with differences in birth timing along allometric trajectories. Prenatal encephalization is shared by all primate radiations, is unique to the primate Order, and is characterized by: (1) a robust change in early embryonic brain/body proportions, and (2) higher average RGP allometric slopes due to slower fetal body growth. While high slopes are observed in several nonprimate species, primates alone exhibit an intercept shift at 1 g body size. This suggests that primate prenatal encephalization is a consequence of early changes to embryonic neural and somatic tissue growth in primates that remain poorly understood.

Self-Reported Sexual Behavioral Interests and Polymorphisms in the Dopamine Receptor D4 (DRD4) Exon III VNTR in Heterosexual Young Adults.

Polymorphisms in the dopamine D4 receptor (DRD4) have previously been shown to associate with a variety of human behavioral phenotypes, including ADHD pathology, alcohol and tobacco craving, financial risk-taking in males, and broader personality traits such as novelty seeking. Recent research has linked the presence of a 7-repeat (7R) allele in a 48-bp variable number of tandem repeats (VNTR) along exon III of DRD4 to age at first sexual intercourse, sexual desire, arousal and function, and infidelity and promiscuity. We hypothesized that carriers of longer DRD4 alleles may report interest in a wider variety of sexual behaviors and experiences than noncarriers. Participants completed a 37-item questionnaire measuring sexual interests as well as Cloninger's Temperament and Character Inventory, and were genotyped for the 48-bp VNTR on exon III of DRD4. Based on our final genotyped sample of female (n = 139) and male (n = 115) participants, we found that 7R carriers reported interest in a wider variety of sexual behaviors (r = 0.16) within a young adult heterosexual sample of European descent. To our knowledge, this is the first reported association between DRD4 exon III VNTR genotype and interest in a variety of sexual behaviors. We discuss these findings within the context of DRD4 research and broader trends in human evolutionary history.