Retinal ganglion cell topography and spatial resolving power in African megachiropterans: Influence of roosting microhabitat and foraging.

Megachiropteran bats (megabats) show remarkable diversity in microhabitat occupation and trophic specializations, but information on how vision relates to their behavioral ecology is scarce. Using stereology and retinal wholemounts, we measured the topographic distribution of retinal ganglion cells and determined the spatial resolution of eight African megachiropterans with distinct roosting and feeding ecologies. We found that species roosting in open microhabitats have a pronounced streak of high retinal ganglion cell density, whereas those favoring more enclosed microhabitats have a less pronounced streak (or its absence in Hypsignathus monstrosus). An exception is the cave-dwelling Rousettus aegyptiacus, which has a pronounced horizontal streak that potentially correlates with its occurrence in more open environments during foraging. In all species, we found a temporal area with maximum retinal ganglion cell density (∼5,000-7,000 cells/mm2 ) that affords enhanced resolution in the frontal visual field. Our estimates of spatial resolution based on peak retinal ganglion cell density and eye size (∼6-12 mm in axial length) range between ∼2 and 4 cycles/degree. Species that occur in more enclosed microhabitats and feed on plant material have lower spatial resolution (∼2 cycles/degree) compared with those that roost in open and semiopen areas (∼3-3.8 cycles/degree). We suggest that the larger eye and concomitant higher spatial resolution (∼4 cycles/degree) in H. monstrosus may have facilitated the carnivorous aspect of its diet. In conclusion, variations in the topographic organization and magnitude of retinal ganglion density reflect the specific ecological needs to detect food/predators and the structural complexity of the environments. J. Comp. Neurol. 525:186-203, 2017. © 2016 Wiley Periodicals, Inc.

The Distribution of Ki-67 and Doublecortin Immunopositive Cells in the Brains of Three Microchiropteran Species, Hipposideros fuliginosus, Triaenops persicus, and Asellia tridens.

This study uses Ki-67 and doublecortin (DCX) immunohistochemistry to delineate potential neurogenic zones, migratory pathways, and terminal fields associated with adult neurogenesis in the brains of three microchiropterans. As with most mammals studied to date, the canonical subgranular and subventricular neurogenic zones were observed. Distinct labeling of newly born cells and immature neurons within the dentate gyrus of the hippocampus was observed in all species. A distinct rostral migratory stream (RMS) that appears to split around the medial aspect of the caudate nucleus was observed. These two rostral stream divisions appear to merge at the rostroventral corner of the caudate nucleus to turn and enter the olfactory bulb, where a large terminal field of immature neurons was observed. DCX immunolabeled neurons were observed mostly in the rostral neocortex, but a potential migratory stream to the neocortex was not identified. A broad swathe of newly born cells and immature neurons was found between the caudoventral division of the RMS and the piriform cortex. In addition, occasional immature neurons were observed in the amygdala and DCX-immunopositive axons were observed in the anterior commissure. While the majority of these features have been found in several mammal species, the large number of DCX immunolabeled cells found between the RMS and the piriform cortex and the presence of DCX immunostained axons in the anterior commissure are features only observed in microchiropterans and insectivores to date. In the diphyletic scenario of chiropteran evolution, these observations align the microchiropterans with the insectivores. Anat Rec, 299:1548-1560, 2016. © 2016 Wiley Periodicals, Inc.

Nuclear organisation of some immunohistochemically identifiable neural systems in five species of insectivore-Crocidura cyanea, Crocidura olivieri, Sylvisorex ollula, Paraechinus aethiopicus and Atelerix frontalis.

The organization of the cholinergic, catecholaminergic, and serotonergic neurons in the brains of five species of insectivores and the orexinergic (hypocretinergic) system in four insectivore species is presented. We aimed to investigate the nuclear complement of these neural systems in comparison to those of other mammalian species. Brains of insectivores were coronally sectioned and immunohistochemically stained with antibodies against choline acetyltransferase, tyrosine hydroxylase, serotonin and orexin-A. The majority of nuclei were similar among the species investigated and to mammals in general, but certain differences in the nuclear complement highlighted potential phylogenetic interrelationships. In the cholinergic system, the three shrew species lacked parabigeminal and Edinger-Westphal nuclei. In addition, the appearance of the laterodorsal tegmental nucleus in all insectivores revealed a mediodorsal arch. All three of these features are the same as those present in microchiropterans. The catecholaminergic system of the three shrew species lacked the A4 and A15d nuclei, as well as having an incipient A9v nucleus, again features found in microchiropteran brains. The serotonergic and orexinergic systems of the insectivores are similar to those seen across most eutherian mammals. The analysis of similarities and differences across mammalian species indicates a potential phylogenetic relationship between the Soricidae (shrews) and the microchiropterans.

Organization of cholinergic, catecholaminergic, serotonergic and orexinergic nuclei in three strepsirrhine primates: Galago demidoff, Perodicticus potto and Lemur catta.

The nuclear organization of the cholinergic, catecholaminergic, serotonergic and orexinergic systems in the brains of three species of strepsirrhine primates is presented. We aimed to investigate the nuclear complement of these neural systems in comparison to those of simian primates, megachiropterans and other mammalian species. The brains were coronally sectioned and immunohistochemically stained with antibodies against choline acetyltransferase, tyrosine hydroxylase, serotonin and orexin-A. The nuclei identified were identical among the strepsirrhine species investigated and identical to previous reports in simian primates. Moreover, a general similarity to other mammals was found, but specific differences in the nuclear complement highlighted potential phylogenetic interrelationships. The central feature of interest was the structure of the locus coeruleus complex in the primates, where a central compactly packed core (A6c) of tyrosine hydroxylase immunopositive neurons was surrounded by a shell of less densely packed (A6d) tyrosine hydroxylase immunopositive neurons. This combination of compact and diffuse divisions of the locus coeruleus complex is only found in primates and megachiropterans of all the mammalian species studied to date. This neural character, along with variances in a range of other neural characters, supports the phylogenetic grouping of primates with megachiropterans as a sister group.

Nuclear organization of some immunohistochemically identifiable neural systems in two species of the Euarchontoglires: A Lagomorph, Lepus capensis, and a Scandentia, Tupaia belangeri.

The present study describes the organization of the nuclei of the cholinergic, catecholaminergic, serotonergic and orexinergic systems in the brains of two members of Euarchontoglires, Lepus capensis and Tupaia belangeri. The aim of the present study was to investigate the nuclear complement of these neural systems in comparison to previous studies on Euarchontoglires and generally with other mammalian species. Brains were coronally sectioned and immunohistochemically stained with antibodies against choline acetyltransferase, tyrosine hydroxylase, serotonin and orexin-A. The majority of nuclei revealed in the current study were similar between the species investigated and to mammals generally, but certain differences in the nuclear complement highlight potential phylogenetic interrelationships within the Euarchontoglires and across mammals. In the northern tree shrew the nucleus of the trapezoid body contained neurons immunoreactive to the choline acetyltransferase antibody with some of these neurons extending into the lamellae within the superior olivary nuclear complex (SON). The cholinergic nature of the neurons of this nucleus, and the extension of cholinergic neurons into the SON, has not been noted in any mammal studied to date. In addition, cholinergic neurons forming the medullary tegmental field were also present in the northern tree shrew. Regarding the catecholaminergic system, the cape hare presented with the rodent specific rostral dorsal midline medullary nucleus (C3), and the northern tree shrew lacked both the ventral and dorsal divisions of the anterior hypothalamic group (A15v and A15d). Both species were lacking the primate/megachiropteran specific compact portion of the locus coeruleus complex (A6c). The nuclei of the serotonergic and orexinergic systems of both species were similar to those seen across most Eutherian mammals. Our results lend support to the monophyly of the Glires, and more broadly suggest that the megachiropterans are more closely related to the primates than are any other members of Euarchontoglires studied to date.

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.

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.

Visual acuity and heterogeneities of retinal ganglion cell densities and the tapetum lucidum of the African elephant (Loxodonta africana).

The eyes of three adult male African elephants were examined, the retinas were whole-mounted, stained and analyzed to determine visual acuity. A range of small to large ganglion cell types were observed across the retinas. We observed three regions of high ganglion cell density, one in the upper temporal quadrant, a visual or horizontal streak and a smaller region at the nasal end of the horizontal streak. The peak density of ganglion cells observed was 5,280/mm(2), and our calculations indicate that the elephant has a maximal visual acuity of between 13.16 and 14.37 cycles/degree. We observed a heterogeneous structure of a tapetum lucidum, the cells of which were found to be most strongly aggregated behind the temporal and nasal densities of retinal ganglion cells. The strength of the tapetum lucidum was weaker posterior to the density of ganglion cells forming the horizontal streak. The morphology of the elephant eye appears to be such that it reflects: (1) the importance of trunk-eye co-ordination for feeding; (2) the importance of 24-hour vigilance for either predators or conspecifics, and (3) the arrhythmic nature of the daily activity of this animal, being useful both diurnally and nocturnally.

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.

Nuclear organization of cholinergic, putative catecholaminergic and serotonergic systems in the brains of two megachiropteran species.

The nuclear organization of the cholinergic, putative catecholaminergic and serotonergic systems within the brains of the megachiropteran straw-coloured fruit bat (Eidolon helvum) and Wahlberg's epauletted fruit bat (Epomophorus wahlbergi) were identified following immunohistochemistry for cholineacetyltransferase, tyrosine hydroxylase and serotonin. The aim of the present study was to investigate possible differences in the nuclear complement of the neuromodulatory systems of these species in comparison to previous studies on megachiropterans, microchiropterans and other mammals. The nuclear organization of these systems is identical to that described previously for megachiropterans and shows many similarities to other mammalian species, especially primates; for example, the putative catecholaminergic system in both species presented a very compact nucleus within the locus coeruleus (A6c) which is found only in megachiropterans and primates. A cladistic analysis of 38 mammalian species and 82 characters from these systems show that megachiropterans form a sister group with primates to the exclusion of other mammals, including microchiropterans. Moreover, the results indicate that megachiropterans and microchiropterans have no clear phylogenetic relationship to each other, as the microchiropteran systems are most closely associated with insectivores. Thus a diphyletic origin of Chiroptera is supported by the present neural findings.

Genetic contribution to individual variation in binocular rivalry rate.

Binocular rivalry occurs when conflicting images are presented in corresponding locations of the two eyes. Perception alternates between the images at a rate that is relatively stable within individuals but that varies widely between individuals. The determinants of this variation are unknown. In addition, slow binocular rivalry has been demonstrated in bipolar disorder, a psychiatric condition with high heritability. The present study therefore examined whether there is a genetic contribution to individual variation in binocular rivalry rate. We employed the twin method and studied both monozygotic (MZ) twins (n = 128 pairs) who are genetically identical, and dizygotic (DZ) twins (n = 220 pairs) who share roughly half their genes. MZ and DZ twin correlations for binocular rivalry rate were 0.51 and 0.19, respectively. The best-fitting genetic model showed 52% of the variance in binocular rivalry rate was accounted for by additive genetic factors. In contrast, nonshared environmental influences accounted for 18% of the variance, with the remainder attributed to measurement error. This study therefore demonstrates a substantial genetic contribution to individual variation in binocular rivalry rate. The results support the vigorous pursuit of genetic and molecular studies of binocular rivalry and further characterization of slow binocular rivalry as an endophenotype for bipolar disorder.

Retinal ganglion cell density of the black rhinoceros (Diceros bicornis): calculating visual resolution.

A single right retina from a black rhinoceros was whole mounted, stained and analyzed to determine the visual resolution of the rhinoceros, an animal with reputedly poor eyesight. A range of small (15-microm diameter) to large (100-microm diameter) ganglion cell types was seen across the retina. We observed two regions of high density of retinal ganglion cells at either end of a long, but thin, horizontal streak. The temporal specialization, which receives light from the anterior visual field, exhibited a ganglion cell density of approximately 2000/mm2, while the nasal specialization exhibited a density of approximately 1500/mm2. The retina exhibited a ganglion cell density bias toward the upper half, especially so, the upper temporal quadrant, indicating that the rhinoceros would be processing visual information from the visual field below the anterior horizon for the most part. Our calculations indicate that the rhinoceros has a visual resolution of 6 cycles/degree. While this resolution is one-tenth that of humans (60 cycles/deg) and less than that of the domestic cat (9 cycles/deg), it is comparable to that of the rabbit (6 cycles/deg), and exceeds that seen in a variety of other mammals including seals, dolphins, microbats, and rats. Thus, the reputation of the rhinoceros as a myopic, weakly visual animal is not supported by our observations of the retina. We calculate that the black rhinoceros could readily distinguish a 30 cm wide human at a distance of around 200 m given the appropriate visual background.

The changing face of perceptual rivalry.

Functional brain-imaging studies of house-face binocular rivalry and Rubin's vase-faces illusion have consistently reported face perception-dependent activity in the right fusiform gyrus. Here we use Rubin's illusion and report that activation of the left hemisphere by caloric vestibular stimulation increases the predominance of the faces percept in a substantial number of test subjects. While partially supporting the brain-imaging lateralization reports, our findings also challenge these studies by suggesting that neural mechanisms of Rubin's illusion cannot be limited to extrastriate perception-dependent processing. In accordance with our previously proposed interhemispheric switch model, the present findings support the notion that perceptual rivalry engages high-level cortical structures that mediate unihemispheric attentional selection.

Psilocybin links binocular rivalry switch rate to attention and subjective arousal levels in humans.

RATIONALE: Binocular rivalry occurs when different images are simultaneously presented to each eye. During continual viewing of this stimulus, the observer will experience repeated switches between visual awareness of the two images. Previous studies have suggested that a slow rate of perceptual switching may be associated with clinical and drug-induced psychosis. OBJECTIVES: The objective of the study was to explore the proposed relationship between binocular rivalry switch rate and subjective changes in psychological state associated with 5-HT2A receptor activation. MATERIALS AND METHODS: This study used psilocybin, the hallucinogen found naturally in Psilocybe mushrooms that had previously been found to induce psychosis-like symptoms via the 5-HT2A receptor. The effects of psilocybin (215 microg/kg) were considered alone and after pretreatment with the selective 5-HT2A antagonist ketanserin (50 mg) in ten healthy human subjects. RESULTS: Psilocybin significantly reduced the rate of binocular rivalry switching and increased the proportion of transitional/mixed percept experience. Pretreatment with ketanserin blocked the majority of psilocybin's "positive" psychosis-like hallucinogenic symptoms. However, ketanserin had no influence on either the psilocybin-induced slowing of binocular rivalry or the drug's "negative-type symptoms" associated with reduced arousal and vigilance. CONCLUSIONS: Together, these findings link changes in binocular rivalry switching rate to subjective levels of arousal and attention. In addition, it suggests that psilocybin's effect on binocular rivalry is unlikely to be mediated by the 5-HT2A receptor.

Caloric vestibular stimulation reveals discrete neural mechanisms for coherence rivalry and eye rivalry: a meta-rivalry model.

Binocular rivalry is an extraordinary visual phenomenon that has engaged investigators for centuries. Since its first report, there has been vigorous debate over how the brain achieves the perceptual alternations that occur when conflicting images are presented simultaneously, one to each eye. Opposing high-level/stimulus-representation models and low-level/eye-based models have been proposed to explain the phenomenon, recently merging into an amalgam view. Here, we provide evidence that during viewing of Díaz-Caneja stimuli, coherence rivalry -- in which aspects of each eye's presented image are perceptually regrouped into rivalling coherent images -- and eye rivalry operate via discrete neural mechanisms. We demonstrate that high-level brain activation by unilateral caloric vestibular stimulation shifts the predominance of perceived coherent images (coherence rivalry) but not half-field images (eye rivalry). This finding suggests that coherence rivalry (like conventional rivalry according to our previous studies) is mediated by interhemispheric switching at a high level, while eye rivalry is mediated by intrahemispheric mechanisms, most likely at a low level. Based on the present data, we further propose that Díaz-Caneja stimuli induce 'meta-rivalry' whereby the discrete high- and low-level competitive processes themselves rival for visual consciousness.

Plaid motion rivalry: correlates with binocular rivalry and positive mood state.

Recently Hupé and Rubin (2003, Vision Research 43 531- 548) re-introduced the plaid as a form of perceptual rivalry by using two sets of drifting gratings behind a circular aperture to produce quasi-regular perceptual alternations between a coherent moving plaid of diamond-shaped intersections and the two sets of component 'sliding' gratings. We call this phenomenon plaid motion rivalry (PMR), and have compared its temporal dynamics with those of binocular rivalry in a sample of subjects covering a wide range of perceptual alternation rates. In support of the proposal that all rivalries may be mediated by a common switching mechanism, we found a high correlation between alternation rates induced by PMR and binocular rivalry. In keeping with a link discovered between the phase of rivalry and mood, we also found a link between PMR and an individual's mood state that is consistent with suggestions that each opposing phase of rivalry is associated with one or the other hemisphere, with the 'diamonds' phase of PMR linked with the 'positive' left hemisphere.

Using psilocybin to investigate the relationship between attention, working memory, and the serotonin 1A and 2A receptors.

Increasing evidence suggests a link between attention, working memory, serotonin (5-HT), and prefrontal cortex activity. In an attempt to tease out the relationship between these elements, this study tested the effects of the hallucinogenic mixed 5-HT1A/2A receptor agonist psilocybin alone and after pretreatment with the 5-HT2A antagonist ketanserin. Eight healthy human volunteers were tested on a multiple-object tracking task and spatial working memory task under the four conditions: placebo, psilocybin (215 microg/kg), ketanserin (50 mg), and psilocybin and ketanserin. Psilocybin significantly reduced attentional tracking ability, but had no significant effect on spatial working memory, suggesting a functional dissociation between the two tasks. Pretreatment with ketanserin did not attenuate the effect of psilocybin on attentional performance, suggesting a primary involvement of the 5-HT1A receptor in the observed deficit. Based on physiological and pharmacological data, we speculate that this impaired attentional performance may reflect a reduced ability to suppress or ignore distracting stimuli rather than reduced attentional capacity. The clinical relevance of these results is also discussed.

Optical imaging of functional organization of V1 and V2 in marmoset visual cortex.

Using optical imaging of intrinsic cortical signals, we examined the functional organization of visual cortical areas V1 and V2 of the marmoset (Callithrix jacchus). Previous studies have reported that adult marmosets do not have ocular dominance columns (ODCs); however, recent studies have called this into question. Using optical imaging methods, we examined whether ODCs could be detected in adult marmosets. We found evidence for functional ODCs in some marmosets but not in others. The activation patterns, when present, were relatively weak and appeared as a mosaic of irregular bands or islands. Consistent with studies in other New World monkeys, these data suggest the presence of ODC variability within the marmoset population. Orientation maps in V1 revealed iso-orientation domains organized in semicontinuous bands oriented orthogonal to the V1/V2 border, a pattern unlike that in Macaque monkey. The presence of directional preference maps in V1 was also suggested. In V2, similar to V2 in Macaque monkeys, stripe-like regions of orientation selectivity overlay the pale cytochrome oxidase regions of V2; zones not selective for orientation overlay the cytochrome thin stripes. However, unlike Macaques, we did not observe clear evidence for orientation maps overlying thick cytochrome oxidase stripes. In sum, our data suggest that significant organizational differences exist between the organization of V1 and V2 in the marmoset and that of Old World primates. Implications for the establishment of functional ocular dominance columns, the coestablishment of multiple featural maps, and cortical magnification factors are discussed.