Pavel Němec

The Distribution of Toxoplasma gondii Cysts in the Brain of a Mouse with Latent Toxoplasmosis: Implications for the Behavioral Manipulation Hypothesis

Background The highly prevalent parasite Toxoplasma gondii reportedly manipulates rodent behavior to enhance the likelihood of transmission to its definitive cat host. The proximate mechanisms underlying this adaptive manipulation remain largely unclear, though a growing body of evidence suggests that the parasite-entrained dysregulation of dopamine metabolism plays a central role. Paradoxically, the distribution of the parasite in the brain has received only scant attention. Methodology/Principal Findings The distributions of T. gondii cysts and histopathological lesions in the brains of CD1 mice with latent toxoplasmosis were analyzed using standard histological techniques. Mice were infected per orally with 10 tissue cysts of the avirulent HIF strain of T. gondii at six months of age and examined 18 weeks later. The cysts were distributed throughout the brain and selective tropism of the parasite toward a particular functional system was not observed. Importantly, the cysts were not preferentially associated with the dopaminergic system and absent from the hypothalamic defensive system. The striking interindividual differences in the total parasite load and cyst distribution indicate a probabilistic nature of brain infestation. Still, some brain regions were consistently more infected than others. These included the olfactory bulb, the entorhinal, somatosensory, motor and orbital, frontal association and visual cortices, and, importantly, the hippocampus and the amygdala. By contrast, a consistently low incidence of tissue cysts was recorded in the cerebellum, the pontine nuclei, the caudate putamen and virtually all compact masses of myelinated axons. Numerous perivascular and leptomeningeal infiltrations of inflammatory cells were observed, but they were not associated with intracellular cysts. Conclusion/Significance The observed pattern of T. gondii distribution stems from uneven brain colonization during acute infection and explains numerous behavioral abnormalities observed in the chronically infected rodents. Thus, the parasite can effectively change behavioral phenotype of infected hosts despite the absence of well targeted tropism.

Birds have primate-like numbers of neurons in the forebrain

Significance Birds are remarkably intelligent, although their brains are small. Corvids and some parrots are capable of cognitive feats comparable to those of great apes. How do birds achieve impressive cognitive prowess with walnut-sized brains? We investigated the cellular composition of the brains of 28 avian species, uncovering a straightforward solution to the puzzle: brains of songbirds and parrots contain very large numbers of neurons, at neuronal densities considerably exceeding those found in mammals. Because these “extra” neurons are predominantly located in the forebrain, large parrots and corvids have the same or greater forebrain neuron counts as monkeys with much larger brains. Avian brains thus have the potential to provide much higher “cognitive power” per unit mass than do mammalian brains. Some birds achieve primate-like levels of cognition, even though their brains tend to be much smaller in absolute size. This poses a fundamental problem in comparative and computational neuroscience, because small brains are expected to have a lower information-processing capacity. Using the isotropic fractionator to determine numbers of neurons in specific brain regions, here we show that the brains of parrots and songbirds contain on average twice as many neurons as primate brains of the same mass, indicating that avian brains have higher neuron packing densities than mammalian brains. Additionally, corvids and parrots have much higher proportions of brain neurons located in the pallial telencephalon compared with primates or other mammals and birds. Thus, large-brained parrots and corvids have forebrain neuron counts equal to or greater than primates with much larger brains. We suggest that the large numbers of neurons concentrated in high densities in the telencephalon substantially contribute to the neural basis of avian intelligence.

The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex.

We have studied the visual system of subterranean mole-rats of the rodent family Bathyergidae, for which light and vision seem of little importance. The eye diameter varies between 3.5mm in Bathyergus suillus and 1.3mm in Heterocephalus glaber. The small superficial eyes have features typical of sighted animals (clear optics, well-developed pupil and well-organized retina) and appear suited for proper image formation. The retinae are rod-dominated but possess rather high cone proportions of about 10%. The total number of retinal ganglion cells and optic nerve fibres ranges between 6000 in Bathyergus suillus and 2100 in Heliophobius argenteocinereus. Visual acuity (estimated from counts of peak ganglion cell density and axial length of the eye) is low, ranging between 0.3 and 0.5 cycles/degree. The retina projects to all the visual structures described in surface-dwelling sighted rodents. The suprachiasmatic nucleus is large and receives bilateral retinal input. All other visual nuclei are reduced in size and receive almost exclusively contralateral retinal projections of varying magnitude. The primary visual cortex is small and, in comparison to other rodents, displaced laterally. In conclusion, the African mole-rats possess relatively well-developed functional visual subsystems involved in photoperiodicity, form and brightness discrimination. In contrast, visual subsystems involved in coordination of visuomotor reflexes are severely reduced. This pattern suggests the retention of basic visual capabilities. Residual vision may enable subterranean mammals to localize breaches in the burrows that let in light thus providing a cue to enable mole-rats to reseal such entry points and to prevent entry of predators.

Evolution and development of the mammalian cerebral cortex.

Comparative developmental studies of the mammalian brain can identify key changes that can generate the diverse structures and functions of the brain. We have studied how the neocortex of early mammals became organized into functionally distinct areas, and how the current level of cortical cellular and laminar specialization arose from the simpler premammalian cortex. We demonstrate the neocortical organization in early mammals, which helps to elucidate how the large, complex human brain evolved from a long line of ancestors. The radial and tangential enlargement of the cortex was driven by changes in the patterns of cortical neurogenesis, including alterations in the proportions of distinct progenitor types. Some cortical cell populations travel to the cortex through tangential migration whereas others migrate radially. A number of recent studies have begun to characterize the chick, mouse and human and nonhuman primate cortical transcriptome to help us understand how gene expression relates to the development and anatomical and functional organization of the adult neocortex. Although all mammalian forms share the basic layout of cortical areas, the areal proportions and distributions are driven by distinct evolutionary pressures acting on sensory and motor experiences during the individual ontogenies.

Changing and shielded magnetic fields suppress c-Fos expression in the navigation circuit: input from the magnetosensory system contributes to the internal representation of space in a subterranean rodent

The neural substrate subserving magnetoreception and magnetic orientation in mammals is largely unknown. Previous experiments have demonstrated that the processing of magnetic sensory information takes place in the superior colliculus. Here, the effects of magnetic field conditions on neuronal activity in the rodent navigation circuit were assessed by quantifying c-Fos expression. Ansells mole-rats (Fukomys anselli), a mammalian model to study the mechanisms of magnetic compass orientation, were subjected to natural, periodically changing, and shielded magnetic fields while exploring an unfamiliar circular arena. In the undisturbed local geomagnetic field, the exploration of the novel environment and/or nesting behaviour induced c-Fos expression throughout the head direction system and the entorhinal–hippocampal spatial representation system. This induction was significantly suppressed by exposure to periodically changing and/or shielded magnetic fields; discrete decreases in c-Fos were seen in the dorsal tegmental nucleus, the anterodorsal and the laterodorsal thalamic nuclei, the postsubiculum, the retrosplenial and entorhinal cortices, and the hippocampus. Moreover, in inactive animals, magnetic field intensity manipulation suppressed c-Fos expression in the CA1 and CA3 fields of the hippocampus and the dorsal subiculum, but induced expression in the polymorph layer of the dentate gyrus. These findings suggest that key constituents of the rodent navigation circuit contain populations of neurons responsive to magnetic stimuli. Thus, magnetic information may be integrated with multimodal sensory and motor information into a common spatial representation of allocentric space within this circuit.

Magnetic Alignment in Carps: Evidence from the Czech Christmas Fish Market

While magnetoreception in birds has been studied intensively, the literature on magnetoreception in bony fish, and particularly in non-migratory fish, is quite scarce. We examined alignment of common carps (Cyprinus carpio) at traditional Christmas sale in the Czech Republic. The sample comprised measurements of the directional bearings in 14,537 individual fish, distributed among 80 large circular plastic tubs, at 25 localities in the Czech Republic, during 817 sampling sessions, on seven subsequent days in December 2011. We found that carps displayed a statistically highly significant spontaneous preference to align their bodies along the North-South axis. In the absence of any other common orientation cues which could explain this directional preference, we attribute the alignment of the fish to the geomagnetic field lines. It is apparent that the display of magnetic alignment is a simple experimental paradigm of great heuristic potential.

Light Perception in Two Strictly Subterranean Rodents: Life in the Dark or Blue?

Background The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function. Methodology/Principal Finding We used a binary choice test to show that the silvery mole-rat Heliophobius argenteocinereus and the giant mole-rat Fukomys mechowii exhibit a clear photoavoidance response to full-spectrum (“white”), blue and green-yellow light, but no significant reaction to ultraviolet or red light during nest building. The mole-rats thus retain dark/light discrimination capabilities and a capacity to perceive short to medium-wavelength light in the photopic range of intensities. These findings further suggest that the mole-rat S opsin has its absorption maximum in the violet/blue part of the spectrum. The assay did not yield conclusive evidence regarding colour discrimination. To test the putative role of vision in bathyergid anti-predatory behaviour, we examined the reaction of mole-rats to the incidence of light in an artificial burrow system. The presence of light in the burrow effectively induced plugging of the illuminated tunnel. Conclusion/Significance Our findings suggest that the photopic vision is conserved and that low acuity residual vision plays an important role in predator avoidance and tunnel maintenance in the African mole-rats.

Towards the neural basis of magnetoreception: a neuroanatomical approach

After more than two decades of intensive research, the physiological mechanisms of animal magnetoreception remain enigmatic. The primary magnetoreceptors are still unknown and our knowledge of the neural substrate subserving magnetic orientation is meagre. Here we argue that this dismal outcome can be largely attributed to the fact that the potential of recently available neurobiological techniques has not been utilized, review some of these techniques and propose a step by step scenario for future research, concentrating on the heuristic potential of instrumentalizing inducible transcription factors (ITFs) such as Jun, Fos, Fos-related antigens and Krox. ITFs can be used as markers of neuronal activation in experiments on freely moving animals performing magnetically based orientation tasks, in experiments on anaesthetised or restrained animals stimulated magnetically, and in experiments employing treatments that specifically disrupt magnetoreception. Therefore they can serve as tools for identifying neurons involved in the detection and processing of magnetic information. When used in combination with other neurobiological tools, ITFs can also be useful for a more comprehensive description of the involved neural networks, for the identification of magnetoreceptors and, in the case of the photoreceptor-based mechanism, also for studying the involvement of specific light-sensitive molecules in the primary transduction process of magnetoreception. Limitations and pitfalls of the proposed approach are also discussed.

Magnetic compass orientation in two strictly subterranean rodents: learned or species-specific innate directional preference?

SUMMARY Evidence for magnetoreception in mammals remains limited. Magnetic compass orientation or magnetic alignment has been conclusively demonstrated in only a handful of mammalian species. The functional properties and underlying mechanisms have been most thoroughly characterized in Ansells mole-rat, Fukomys anselli, which is the species of choice due to its spontaneous drive to construct nests in the southeastern sector of a circular arena using the magnetic field azimuth as the primary orientation cue. Because of the remarkable consistency between experiments, it is generally believed that this directional preference is innate. To test the hypothesis that spontaneous southeastern directional preference is a shared, ancestral feature of all African mole-rats (Bathyergidae, Rodentia), we employed the same arena assay to study magnetic orientation in two other mole-rat species, the social giant mole-rat, Fukomys mechowii, and the solitary silvery mole-rat, Heliophobius argenteocinereus. Both species exhibited spontaneous western directional preference and deflected their directional preference according to shifts in the direction of magnetic north, clearly indicating that they were deriving directional information from the magnetic field. Because all of the experiments were performed in total darkness, our results strongly suggest that all African mole-rats use a light-independent magnetic compass for near-space orientation. However, the spontaneous directional preference is not common and may be either innate (but species-specific) or learned. We propose an experiment that should be performed to distinguish between these two alternatives.

Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole, Clethrionomys glareolus

Magnetoreception has been convincingly demonstrated in only a few mammalian species. Among rodents, magnetic compass orientation has been documented in four species of subterranean mole rats and two epigeic (i.e. active above ground) species—the Siberian hamster and the C57BL/6J mouse. The mole rats use the magnetic field azimuth to determine compass heading; their directional preference is spontaneous and unimodal, and their magnetic compass is magnetite-mediated. By contrast, the primary component of orientation response is learned in the hamster and the mouse, but both species also exhibit a weak spontaneous bimodal preference in the natural magnetic field. To determine whether the magnetic compass of wild epigeic rodents features the same functional properties as that of laboratory rodents, we investigated magnetic compass orientation in the bank vole Clethrionomys glareolus (Cricetidae, Rodentia). The voles exhibited a robust spontaneous bimodal directional preference, i.e. built nests and slept preferentially along the north-south axis, and deflected their directional preference according to a shift in the direction of magnetic north, clearly indicating that they were deriving directional information from the magnetic field. Thus, bimodal, axially symmetrical directional choice seems to be a common feature shared by epigeic rodents. However, spontaneous directional preference in the bank vole appeared to be more pronounced than that reported in the hamster and the mouse. These findings suggest that bank voles are well suited for future studies investigating the adaptive significance and mechanisms of magnetic orientation in epigeic rodents.