Most cited article - PubMed ID 11598299
Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal
Several groups of mammals use the Earth's magnetic field for orientation, but their magnetosensory organ remains unknown. The Ansell's mole-rat (Fukomys anselli, Bathyergidae, Rodentia) is a microphthalmic subterranean rodent with innate magnetic orientation behaviour. Previous studies on this species proposed that its magnetoreceptors are located in the eye. To test this hypothesis, we assessed magnetic orientation in mole-rats after the surgical removal of their eyes compared to untreated controls. Initially, we demonstrate that this enucleation does not lead to changes in routine behaviours, including locomotion, feeding and socializing. We then studied magnetic compass orientation by employing a well-established nest-building assay under four magnetic field alignments. In line with previous studies, control animals exhibited a significant preference to build nests in magnetic southeast. By contrast, enucleated mole-rats built nests in random magnetic orientations, suggesting an impairment of their magnetic sense. The results provide robust support for the hypothesis that mole-rats perceive magnetic fields with their minute eyes, probably relying on magnetite-based receptors in the cornea.
- Keywords
- animal orientation, magnetic sense, magnetite, mole-rat, sensory biology,
- MeSH
- Locomotion MeSH
- Magnetic Fields MeSH
- Magnetics MeSH
- Mole Rats * MeSH
- Orientation * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
African mole-rats are subterranean rodents that spend their whole life in underground burrow systems. They show a range of morphological and physiological adaptations to their ecotope, for instance severely reduced eyes and specialized somatosensory, olfactory, and auditory systems. These adaptations are also reflected in the accessory sensory pathways in the brain that process the input coming from the sensory organs. So far, a brain atlas was available only for the naked mole-rat (Heterocephalus glaber). The Ansell's mole-rat (Fukomys anselli) has been the subject of many investigations in various disciplines (ethology, sensory physiology, and anatomy) including magnetic orientation. It is therefore surprising that an atlas of the brain of this species was not available so far. Here, we present a comprehensive atlas of the Ansell's mole-rat brain based on Nissl and Klüver-Barrera stained sections. We identify and label 375 brain regions and discuss selected differences from the brain of the closely related naked mole-rat as well as from epigeic mammals (rat), with a particular focus on the auditory brainstem. This atlas can serve as a reference for future neuroanatomical investigations of subterranean mammals.
- Keywords
- Nissl, RRID:SCR_005910, RRID:SCR_014199, auditory system, magnetoreception, nervous system, neuroanatomy, rodent, subterranean mammal,
- MeSH
- Anatomy, Artistic * MeSH
- Atlases as Topic * MeSH
- Mole Rats anatomy & histology MeSH
- Brain anatomy & histology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
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.
- MeSH
- Arvicolinae physiology MeSH
- Nesting Behavior physiology MeSH
- Magnetic Phenomena * MeSH
- Orientation physiology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The dorsolateral area of the hippocampal formation of birds is commonly assumed to play a central role in processing information needed for geographical positioning and homing. Previous work has interpreted odour-induced activity in this region as evidence for an 'olfactory map'. Here, we show, using c-Fos expression as a marker, that neuronal activation in the dorsolateral area of the hippocampal formation of pigeons is primarily a response to odour novelty, not to the spatial distribution of odour sources that would be necessary for an olfactory map. Pigeons exposed to odours had significantly more neurons activated in this area of the brain than pigeons exposed to filtered air with odours removed. This increased activity was observed only in response to unfamiliar odours. No change in activity was observed when pigeons were exposed to home odours. These findings are consistent with non-home odours activating non-olfactory components of the pigeon's navigation system. The pattern of neuronal activation in the triangular and dorsomedial areas of the hippocampal formation was, by contrast, consistent with the possibility that odours play a role in providing spatial information.
- Keywords
- hippocampus, homing, immediate early genes, navigation, olfactory activation, pigeon,
- MeSH
- Olfactory Perception * MeSH
- Columbidae physiology MeSH
- Genetic Markers MeSH
- Hippocampus physiology MeSH
- Odorants * MeSH
- Spatial Navigation MeSH
- Proto-Oncogene Proteins c-fos genetics metabolism MeSH
- Avian Proteins genetics metabolism MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Genetic Markers MeSH
- Proto-Oncogene Proteins c-fos MeSH
- Avian Proteins MeSH
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. Ansell's 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.
- MeSH
- Behavior, Animal MeSH
- Sensation genetics physiology MeSH
- Superior Colliculi metabolism MeSH
- Dentate Gyrus metabolism MeSH
- Hippocampus metabolism MeSH
- Magnetics * MeSH
- Mole Rats genetics metabolism physiology MeSH
- Neural Pathways physiology MeSH
- Orientation MeSH
- Proto-Oncogene Proteins c-fos genetics metabolism MeSH
- Somatosensory Cortex metabolism MeSH
- Space Perception physiology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Proto-Oncogene Proteins c-fos MeSH
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.
- MeSH
- Electromagnetic Fields MeSH
- Genes, fos MeSH
- Magnetics * MeSH
- Nervous System Physiological Phenomena MeSH
- Nervous System anatomy & histology radiation effects MeSH
- Neurons physiology MeSH
- Gene Expression Regulation physiology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
Our previous experiments indicated an age- and sex-dependent functional lateralization of a high-affinity choline uptake system in hippocampi of Wistar rats. The system is connected with acetylcholine synthesis and also plays a role in spatial navigation. The current study demonstrates that a single in vivo exposure of 7- or 14-day-old males to a static magnetic field of 0.14 T for 60-120 min evokes asymmetric alterations in the activity of carriers in adulthood. Namely, the negative field (antiparallel orientation with a vertical component of the geomagnetic field) mediated a more marked decrease in the right hippocampus. The positive field (parallel orientation) was ineffective. Moreover, differences between the carriers from the right and the left hippocampi were observed on synaptosomes pretreated with superparamagnetic nanoparticles and exposed for 30 min in vitro. The positive field enhanced more markedly the activity of carriers from the right hippocampus, the negative that from the left hippocampus, on the contrary. Our results demonstrate functionally teratogenic risks of the alterations in the orientation of the strong static magnetic field for postnatal brain development and suggest functional specialization of both hippocampi in rats. Choline carriers could be involved as secondary receptors in magnetoreception through direct effects of geomagnetic field on intracellular magnetite crystals and nanoparticles applied in vivo should be a useful tool to evaluate magnetoreception in future research.
- MeSH
- Choline metabolism MeSH
- Electromagnetic Fields * MeSH
- Functional Laterality physiology MeSH
- Hippocampus metabolism physiology MeSH
- Kinetics MeSH
- Rats MeSH
- Maternal Deprivation MeSH
- Microspheres MeSH
- Drug Carriers MeSH
- Animals, Newborn physiology MeSH
- Sex Characteristics MeSH
- Rats, Wistar MeSH
- Aging physiology MeSH
- Synaptosomes metabolism MeSH
- In Vitro Techniques MeSH
- Animals MeSH
- Check Tag
- Rats MeSH
- Male MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Choline MeSH
- Drug Carriers MeSH