Activation changes in zebra finch (Taeniopygia guttata) brain areas evoked by alterations of the earth magnetic field

Many animals are able to perceive the earth magnetic field and to use it for orientation and navigation within the environment. The mechanisms underlying the perception and processing of magnetic field information within the brain have been thoroughly studied, especially in birds, but are still obscure. Three hypotheses are currently discussed, dealing with ferromagnetic particles in the beak of birds, with the same sort of particles within the lagena organs, or describing magnetically influenced radical-pair processes within retinal photopigments. Each hypothesis is related to a well-known sensory organ and claims parallel processing of magnetic field information with somatosensory, vestibular and visual input, respectively. Changes in activation within nuclei of the respective sensory systems have been shown previously. Most of these previous experiments employed intensity enhanced magnetic stimuli or lesions. We here exposed unrestrained zebra finches to either a stationary or a rotating magnetic field of the local intensity and inclination. C-Fos was used as an activity marker to examine whether the two treatments led to differences in fourteen brain areas including nuclei of the somatosensory, vestibular and visual system. An ANOVA revealed an overall effect of treatment, indicating that the magnetic field change was perceived by the birds. While the differences were too small to be significant in most areas, a significant enhancement of activation by the rotating stimulus was found in a hippocampal subdivision. Part of the hyperpallium showed a strong, nearly significant, increase. Our results are compatible with previous studies demonstrating an involvement of at least three different sensory systems in earth magnetic field perception and suggest that these systems, probably less elaborated, may also be found in nonmigrating birds.     

The lagena (the third otolith endorgan in vertebrates)

In this review, the structure and functions of the lagena (the third otolith organ) in an evolutionary lineage of the vertebrates are described and discussed. The lagenar macula appears first in the posterior part of the sacculus of elasmobranchs; in these animals, the lagena is considered to be involved in the balance support (orientation with respect to the gravitation force). The lagena as a separate endorgan has been described in teleost fishes; in some species, the lagena is connected with the sacculus, while in other species the interrelations of these structures can be dissimilar. The lagena supplements the functions of the sacculus; in fishes (animals with no special organ of hearing), it is involved in discrimination of sound oscillations, identification of the gravitation vector, and orientation in the course of movements within the vertical plane. In amphibians, the lagena is localized in the posterior part of the sacculus, near the auditory structures; it performs mostly vestibular and (to a much lesser extent) auditory functions. In amniotes, the lagena was first separated from the sacculus; it is localized in the cochlear canal, distally with respect to the hearing organ. Information on the functions of the lagena in amniotes is rather limited and contradictory. Central projections of this organ have been examined practically only in birds. Lagenar afferents project to the vestibular nuclei and cerebellum, while some fibers come to the auditory nuclei of the medulla. The lagena in birds can be related to their navigation abilities (birds are supposed to be capable of orienting within the magnetic field of the Earth due to the magnetic properties of the lagenar otoconia; this structure can also provide detection of movements along the vertical axis. The close proximity between the otolithic and auditory endorgans in the cochlear canal of amniotes can be indicative of the functional significance of these interrelations. This aspect, however, remains at present undiscovered. In mammals (except Monotremata), there is no lagena as an independent endorgan. Neirofiziologiya/Neurophysiology, Vol. 40, No. 2, pp. 160–178, March–April, 2008.     

Theoretical analysis of an iron mineral-based magnetoreceptor model in birds

Sensing the magnetic field has been established as an essential part of navigation and orientation of various animals for many years. Only recently has the first detailed receptor concept for magnetoreception been published based on histological and physical results. The considered mechanism involves two types of iron minerals (magnetite and maghemite) that were found in subcellular compartments within sensory dendrites of the upper beak of several bird species. But so far a quantitative evaluation of the proposed receptor is missing. In this article, we develop a theoretical model to quantitatively and qualitatively describe the magnetic field effects among particles containing iron minerals. The analysis of forces acting between these subcellular compartments shows a particular dependence on the orientation of the external magnetic field. The iron minerals in the beak are found in the form of crystalline maghemite platelets and assemblies of magnetite nanoparticles. We demonstrate that the pull or push to the magnetite assemblies, which are connected to the cell membrane, may reach a value of 0.2 pN -- sufficient to excite specific mechanoreceptive membrane channels in the nerve cell. The theoretical analysis of the assumed magnetoreceptor system in the avian beak skin clearly shows that it might indeed be a sensitive biological magnetometer providing an essential part of the magnetic map for navigation.     

Mechanisms of magnetic orientation in birds

Behavior and electrophysiological studies have demonstrateda sensitivity to characteristics of the Geomagnetic field thatcan be used for navigation, both for direction finding (compass)and position finding (map). The avian magnetic compass receptorappears to be a light-dependent, wavelength-sensitive systemthat functions as a polarity compass (i.e., it distinguishespoleward from equatorward rather than north from south) andis relatively insensitive to changes in magnetic field intensity.The receptor is within the retina and is based on one or morephotopigments, perhaps cryptochromes. A second receptor systemappears to be based on magnetite and might serve to transducelocation information independent of the compass system. Thisreceptor is associated with the ophthalmic branch of the trigeminalnerve and is sensitive to very small (<50 nanotesla) changesin the intensity of the magnetic field. In neither case hasa neuron that responded to changes in the magnetic field beentraced to a structure that can be identified to be a receptor.Almost nothing is known about how magnetic information is processedwithin the brain or how it is combined with other sensory informationand used for navigation. These remain areas of future research.     

生物磁学在鸟类定向研究中的进展

地球上广泛存在的地磁场能够为导航提供可靠的信息,因此很多鸟类在迁徙和归巢过程中都使用地磁信息来保证航行方向的正确,在迁徙的鸟类中已经发现有18种是利用地磁罗盘进行定向和导航的。本文从鸟类使用的磁罗盘、航行地图以及磁感应机制等几方面阐述了目前在鸟类生物磁学方面的研究进展。     

Differential Recruitment of Brain Networks following Route and Cartographic Map Learning of Spatial Environments

An extensive neuroimaging literature has helped characterize the brain regions involved in navigating a spatial environment. Far less is known, however, about the brain networks involved when learning a spatial layout from a cartographic map. To compare the two means of acquiring a spatial representation, participants learned spatial environments either by directly navigating them or learning them from an aerial-view map. While undergoing functional magnetic resonance imaging (fMRI), participants then performed two different tasks to assess knowledge of the spatial environment: a scene and orientation dependent perceptual (SOP) pointing task and a judgment of relative direction (JRD) of landmarks pointing task. We found three brain regions showing significant effects of route vs. map learning during the two tasks. Parahippocampal and retrosplenial cortex showed greater activation following route compared to map learning during the JRD but not SOP task while inferior frontal gyrus showed greater activation following map compared to route learning during the SOP but not JRD task. We interpret our results to suggest that parahippocampal and retrosplenial cortex were involved in translating scene and orientation dependent coordinate information acquired during route learning to a landmark-referenced representation while inferior frontal gyrus played a role in converting primarily landmark-referenced coordinates acquired during map learning to a scene and orientation dependent coordinate system. Together, our results provide novel insight into the different brain networks underlying spatial representations formed during navigation vs. cartographic map learning and provide additional constraints on theoretical models of the neural basis of human spatial representation.     

Reconstructing feedback representations in the ventral visual pathway with a generative adversarial autoencoder

While vision evokes a dense network of feedforward and feedback neural processes in the brain, visual processes are primarily modeled with feedforward hierarchical neural networks, leaving the computational role of feedback processes poorly understood. Here, we developed a generative autoencoder neural network model and adversarially trained it on a categorically diverse data set of images. We hypothesized that the feedback processes in the ventral visual pathway can be represented by reconstruction of the visual information performed by the generative model. We compared representational similarity of the activity patterns in the proposed model with temporal (magnetoencephalography) and spatial (functional magnetic resonance imaging) visual brain responses. The proposed generative model identified two segregated neural dynamics in the visual brain. A temporal hierarchy of processes transforming low level visual information into high level semantics in the feedforward sweep, and a temporally later dynamics of inverse processes reconstructing low level visual information from a high level latent representation in the feedback sweep. Our results append to previous studies on neural feedback processes by presenting a new insight into the algorithmic function and the information carried by the feedback processes in the ventral visual pathway.     

Spontaneous preferences for magnetic compass direction in the American red-spotted newt, <Emphasis Type="Italic">Notophthalmus viridescens</Emphasis> (Salamandridae,Urodela)

In addition to other sensory modalities, migratory vertebrates are able to use the earths’ magnetic field for orientation and navigation. The magnetic cue may also serve as a reference for other orientation mechanisms. In this study, significant evidence is shown that, even in darkness, newts (Notophthalmus viridescens, Salamandridae) spontaneously align according to the natural or to the deviated earth’s magnetic field lines, thereby demonstrating a magnetic compass sensitivity. All newts preferred compass directions close to east or west or chose the E/W axially and hence sought to maintain a specific angle or axis relative to the magnetic field vector. Such an active alignment is considered an essential precondition for magnetic orientation. When the horizontal magnetic vector was experimentally compensated, animals became disoriented. We infer that the animals have either learned the preferred magnetic direction/axis individually or that these choices are innate and could even be seasonally different as in migrating birds. It is still an unanswered question as to how and where the physical and physiological mechanisms of magnetic transduction and reception take place. The visual system and other light-dependent (radical pairs) mechanisms alone are often claimed to be in function, but this must now be reconsidered given the results from animals when deprived of light. The results may therefore point to putative receptor mechanisms involving magnetite elements in specialized magneto-receptors.     

Magnetic orientation and navigation in marine turtles, lobsters, and molluscs: concepts and conundrums

The Earth's magnetic field provides a pervasive source of directionalinformation used by phylogenetically diverse marine animals.Behavioral experiments with sea turtles, spiny lobsters, andsea slugs have revealed that all have a magnetic compass sense,despite vast differences in the environment each inhabits andthe spatial scale over which each moves. For two of these animals,the Earth's field also serves as a source of positional information.Hatchling loggerhead sea turtles from Florida responded to themagnetic fields found in three widely separated regions of theAtlantic Ocean by swimming in directions that would, in eachcase, facilitate movement along the migratory route. Thus, foryoung loggerheads, regional magnetic fields function as navigationalmarkers and elicit changes in swimming direction at crucialgeographic boundaries. Older turtles, as well as spiny lobsters,apparently acquire a "magnetic map" that enables them to usemagnetic topography to determine their position relative tospecific goals. Relatively little is known about the neuralmechanisms that underlie magnetic orientation and navigation.A promising model system is the marine mollusc Tritonia diomedea,which possesses both a magnetic compass and a relatively simplenervous system. Six neurons in the brain of T. diomedea havebeen identified that respond to changes in magnetic fields.At least some of these appear to be ciliary motor neurons thatgenerate or modulate the final behavioral output of the orientationcircuitry. These findings represent an encouraging step towarda holistic understanding of the cells and circuitry that underliemagnetic orientation behavior in one model organism.     

Common Cortical Loci Are Activated during Visuospatial Interpolation and Orientation Discrimination Judgements

There is a wealth of literature on the role of short-range interactions between low-level orientation-tuned filters in the perception of discontinuous contours. However, little is known about how spatial information is integrated across more distant regions of the visual field in the absence of explicit local orientation cues, a process referred to here as visuospatial interpolation (VSI). To examine the neural correlates of VSI high field functional magnetic resonance imaging was used to study brain activity while observers either judged the alignment of three Gabor patches by a process of interpolation or discriminated the local orientation of the individual patches. Relative to a fixation baseline the two tasks activated a largely over-lapping network of regions within the occipito-temporal, occipito-parietal and frontal cortices. Activated clusters specific to the orientation task (orientation>interpolation) included the caudal intraparietal sulcus, an area whose role in orientation encoding per se has been hotly disputed. Surprisingly, there were few task-specific activations associated with visuospatial interpolation (VSI>orientation) suggesting that largely common cortical loci were activated by the two experimental tasks. These data are consistent with previous studies that suggest higher level grouping processes -putatively involved in VSI- are automatically engaged when the spatial properties of a stimulus (e.g. size, orientation or relative position) are used to make a judgement.     

Neural induction in the absence of organizer in salamanders is mediated by MAPK

Research on the mechanisms of embryonic induction had a great setback in the 1940s when Barth discovered and Holtfreter confirmed that ectoderm of Ambystoma maculatum salamander embryos could form brain tissue when cultured in a simple saline solution. We have revisited this classical experiment and found that when cultured animal cap ectoderm attaches to a glass substratum, it can self-organize to form complex organs such as brain vesicles, eyes, lens and olfactory placodes. Only anterior neural organs were generated. Under these culture conditions ERK became diphosphorylated, indicating a sustained activation of the Ras/MAPK pathway. Using sand particles as an example of a heterologous neural inducer similar results were obtained. Addition of U0126, a specific antagonist of MEK, the enzyme that phosphorylates ERK/MAPK, inhibited neural differentiation. The closely related control compound U0124 had no effect. We conclude that neural induction in the absence of organizer in A. maculatum requires Ras/MAPK-activation. These findings provide a molecular explanation for the activity of heterologous neural inducers that dominated thinking in amphibian experimental embryology for many decades.     

Structural variation in the inner ears of four deep-sea elopomorph fishes

Deep-sea fishes have evolved in dark or dimly lit environments devoid of the visual cues available to shallow-water species. Because of the limited opportunity for visual scene analysis by deep-sea fishes, it is reasonable to hypothesize that the inner ears of at least some such species may have evolved structural adaptations to enhance hearing capabilities in lieu of vision. As an initial test of this hypothesis, scanning electron microscopy was used to examine the structure of the inner ears of four deep-sea elopomorph species inhabiting different depths: Synaphobranchus kaupii, Synaphobranchus bathybius, Polyacanthonotus challengeri, and Halosauropsis macrochir. The shape of the sensory epithelia and hair cell ciliary bundle orientation of the saccule, lagena, and utricle, the three otolithic organs associated with audition and vestibular function, are described. The saccules of all four species have a common, alternating ciliary bundle orientation pattern. In contrast, the lagena exhibits more interspecific diversity in shape and ciliary bundle orientation, suggesting that it has special adaptations in these species. The macula neglecta, a sensory epithelium of unknown function, is present in all four species.     

Bats respond to polarity of a magnetic field

Bats have been shown to use information from the Earth's magnetic field during orientation. However, the mechanism underlying this ability remains unknown. In this study we investigated whether bats possess a polarity- or inclination-based compass that could be used in orientation. We monitored the hanging position of adult Nyctalus plancyi in the laboratory in the presence of an induced magnetic field of twice Earth-strength. When under the influence of a normally aligned induced field the bats showed a significant preference for hanging at the northern end of their roosting basket. When the vertical component of the field was reversed, the bats remained at the northern end of the basket. However, when the horizontal component of the field was reversed, the bats changed their positions and hung at the southern end of the basket. Based on these results, we conclude that N. plancyi, unlike all other non-mammalian vertebrates tested to date, uses a polarity-based compass during orientation in the roost, and that the same compass is also likely to underlie bats' long-distance navigation abilities.     

Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame

The ability to orient and navigate through the terrestrial environment represents a computational challenge common to all vertebrates. It arises because motion sensors in the inner ear, the otolith organs, and the semicircular canals transduce self-motion in an egocentric reference frame. As a result, vestibular afferent information reaching the brain is inappropriate for coding our own motion and orientation relative to the outside world. Here we show that cerebellar cortical neuron activity in vermal lobules 9 and 10 reflects the critical computations of transforming head-centered vestibular afferent information into earth-referenced self-motion and spatial orientation signals. Unlike vestibular and deep cerebellar nuclei neurons, where a mixture of responses was observed, Purkinje cells represent a homogeneous population that encodes inertial motion. They carry the earth-horizontal component of a spatially transformed and temporally integrated rotation signal from the semicircular canals, which is critical for computing head attitude, thus isolating inertial linear accelerations during navigation.     

鸟类磁感受的生物物理机制研究进展

行为学实验表明,许多鸟类能够感受到地磁信息,并利用地磁信息完成迁徙或归巢。地磁场信息能提供可靠导航信息,磁力线可提供罗盘信息,而磁场强度和倾角可提供位置信息。文章介绍了鸟类磁感受机制的两种重要假说——基于磁铁矿的磁感受假说和化学磁感受假说,阐明了两种假说的理论原理及实验证据,对地磁信息传导神经通路与处理脑区做了评述,并展望了其发展方向。     

Neurophysiological properties of magnetic cells in the pigeon's visual system

Summary Single unit electrical activity was recorded extracellularly in the nucleus of the basal optic root (nBOR) and in the optic tectum under earth-strength magnetic stimulation. Units in the nBOR which were stimulated while the eyes were illuminated by light of different wavelengths exhibited peaks of magnetic responsiveness at 503 nm and 582 nm.Magnetically directional selective cells were found in the stratum griseum et fibrosum superficiale of the optic tectum. They also showed directional selectivity to dynamic photic stimuli. Response peaks varied with the orientation of the pigeon in the horizontal plane. This confirmed that the magnetic responses contained directional information. The results suggest that the receptor and neural organisation of the pigeon's visual system provides an adequate substrate for the detection and elaboration of magnetic compass information.     

Orientation of paramecium swimming in a DC magnetic field

We found that a ciliated protozoan, Paramecium, swam perpendicular to a static (DC) magnetic field (0.68 T). The swimming orientation was similar even when the ionic current through the cell membrane disappeared after saponin treatment. To determine the diamagnetic anisotropy of intracellular organs, macronuclei, cilia, and secretory vesicles, trichocysts, were selectively isolated. Both cilia and trichocysts tended to align their long axis parallel to the magnetic field (0.78 T). Paramecium mutants that lack trichocysts also swam perpendicular to the magnetic field, although the proportion fraction was smaller than the normal population. Since large numbers of cilia and trichocysts are arranged at right angles to the long axis of the cell, the diamagnetic anisotropies of cilia and trichocysts cause the long axis of the cell to align perpendicular to the magnetic field. In contrast to the DC magnetic field, an alternative (AC) magnetic field (60 Hz, 0.65 T) had almost no effect on the swimming orientation of Paramecium.     

Resolution of uncertainty in prefrontal cortex

Making optimal decisions in the face of uncertain or incomplete information arises as a common problem in everyday behavior, but the neural processes underlying this ability remain poorly understood. A typical case is navigation, in which a subject has to search for a known goal from an unknown location. Navigating under uncertain conditions requires making decisions on the basis of the current belief about location and updating that belief based on incoming information. Here, we use functional magnetic resonance imaging during a maze navigation task to study neural activity relating to the resolution of uncertainty as subjects make sequential decisions to reach a goal. We show that distinct regions of prefrontal cortex are engaged in specific computational functions that are well described by a Bayesian model of decision making. This permits efficient goal-oriented navigation and provides new insights into decision making by humans.     

A neural systems analysis of adaptive navigation

In the field of the neurobiology of learning, significant emphasis has been placed on understanding neural plasticity within a single structure (or synapse type) as it relates to a particular type of learning mediated by a particular brain area. To appreciate fully the breadth of the plasticity responsible for complex learning phenomena, it is imperative that we also examine the neural mechanisms of the behavioral instantiation of learned information, how motivational systems interact, and how past memories affect the learning process. To address this issue, we describe a model of complex learning (rodent adaptive navigation) that could be used to study dynamically interactive neural systems. Adaptive navigation depends on the efficient integration of external and internal sensory information with motivational systems to arrive at the most effective cognitive and/or behavioral strategies. We present evidence consistent with the view that during navigation: 1) the limbic thalamus and limbic cortex is primarily responsible for the integration of current and expected sensory information, 2) the hippocampal-septal-hypothalamic system provides a mechanism whereby motivational perspectives bias sensory processing, and 3) the amygdala-prefrontal-striatal circuit allows animals to evaluate the expected reinforcement consequences of context-dependent behavioral responses. Although much remains to be determined regarding the nature of the interactions among neural systems, new insights have emerged regarding the mechanisms that underlie flexible and adaptive behavioral responses.     

Modality-independent coding of spatial layout in the human brain

In many nonhuman species, neural computations of navigational information such as position and orientation are not tied to a specific sensory modality [1, 2]. Rather, spatial signals are integrated from multiple input sources, likely leading to abstract representations of space. In contrast, the potential for abstract spatial representations in humans is not known, because most neuroscientific experiments on human navigation have focused exclusively on visual cues. Here, we tested the modality independence hypothesis with two functional magnetic resonance imaging (fMRI) experiments that characterized computations in regions implicated in processing spatial layout [3]. According to the hypothesis, such regions should be recruited for spatial computation of 3D geometric configuration, independent of a specific sensory modality. In support of this view, sighted participants showed strong activation of the parahippocampal place area (PPA) and the retrosplenial cortex (RSC) for visual and haptic exploration of information-matched scenes but not objects. Functional connectivity analyses suggested that these effects were not related to visual recoding, which was further supported by a similar preference for haptic scenes found with blind participants. Taken together, these findings establish the PPA/RSC network as critical in modality-independent spatial computations and provide important evidence for a theory of high-level abstract spatial information processing in the human brain.