ABSTRACT
For many animals, faces are a vitally important visual stimulus. Hence, it is not surprising that face perception has become a very popular research topic in neuroscience, with ca. 2000 papers published every year. As a result, significant progress has been made in understanding the intricate mechanisms underlying this phenomenon. However, the ontogeny of face perception, in particular the role of innate predispositions, remains largely unexplored at the neural level. Several influential studies in monkeys have suggested that seeing faces is necessary for the development of the face-selective brain domains. At the same time, behavioural experiments with newborn human babies and newly-hatched domestic chicks demonstrate that a spontaneous preference towards faces emerges early in life without pre-existing experience. Moreover, we were recently able to record face-selective neural responses in the brain of young, face-naïve chicks, thus demonstrating the existence of an innate face detection mechanism. In this review, we discuss these seemingly contradictory results and propose potential experimental approaches to resolve some of the open questions.
ABSTRACT
Sensory stimulation during the prenatal period has been argued to be a main factor in establishing asymmetry in the vertebrate brain. However, though largely studied in behavior and neuroanatomy, nothing is known on the effects of light stimulation in embryo on the activities of single neurons. We performed single-unit recordings from the left and right entopallium of dark- and light-incubated chicks, following ipsi-, contra-, and bilateral visual stimulation. Light incubation increased the general responsiveness of visual neurons in both the left and the right entopallium. Entopallial responses were clearly lateralized in dark-incubated chicks, which showed a general right-hemispheric dominance. This could be suppressed or inverted after light incubation, revealing the presence of both spontaneous and light-dependent asymmetries. These results suggest that asymmetry in single-neuron activity is present at the onset and can be modulated by environmental stimuli such as light exposure in embryos.
ABSTRACT
Migratory songbirds have the remarkable ability to extract directional information from the Earth's magnetic field1,2. The exact mechanism of this light-dependent magnetic compass sense, however, is not fully understood. The most promising hypothesis focuses on the quantum spin dynamics of transient radical pairs formed in cryptochrome proteins in the retina3-5. Frustratingly, much of the supporting evidence for this theory is circumstantial, largely because of the extreme challenges posed by genetic modification of wild birds. Drosophila has therefore been recruited as a model organism, and several influential reports of cryptochrome-mediated magnetic field effects on fly behaviour have been widely interpreted as support for a radical pair-based mechanism in birds6-23. Here we report the results of an extensive study testing magnetic field effects on 97,658 flies moving in a two-arm maze and on 10,960 flies performing the spontaneous escape behaviour known as negative geotaxis. Under meticulously controlled conditions and with vast sample sizes, we have been unable to find evidence for magnetically sensitive behaviour in Drosophila. Moreover, after reassessment of the statistical approaches and sample sizes used in the studies that we tried to replicate, we suggest that many-if not all-of the original results were false positives. Our findings therefore cast considerable doubt on the existence of magnetic sensing in Drosophila and thus strongly suggest that night-migratory songbirds remain the organism of choice for elucidating the mechanism of light-dependent magnetoreception.
Subject(s)
Drosophila melanogaster , Magnetic Fields , Negative Results , Animals , Animal Migration , Cryptochromes/metabolism , Songbirds/physiology , Drosophila melanogaster/physiology , Models, Animal , Escape Reaction , Maze Learning , Sample Size , LightABSTRACT
Perception of numerousness, i.e. number of items in a set, is an important cognitive ability, which is present in several animal taxa. In spite of obvious differences in neuroanatomy, insects, fishes, reptiles, birds, and mammals all possess a "number sense". Furthermore, information regarding numbers can belong to different sensory modalities: animals can estimate a number of visual items, a number of tones, or a number of their own movements. Given both the heterogeneity of stimuli and of the brains processing these stimuli, it is hard to imagine that number cognition can be traced back to the same evolutionary conserved neural pathway. However, neurons that selectively respond to the number of stimuli have been described in higher-order integration brain centres both in primates and in birds, two evolutionary distant groups. Although most probably not of the same evolutionary origin, these number neurons share remarkable similarities in their response properties. Instead of homology, this similarity might result from computational advantages of the underlying coding mechanism. This means that one might expect numerousness information to undergo similar steps of neural processing even in evolutionary distant neural pathways. Following this logic, in this review we summarize our current knowledge of how numerousness is processed in the brain from sensory input to coding of abstract information in the higher-order integration centres. We also propose a list of key open questions that might promote future research on number cognition.
Subject(s)
Brain , Cognition , Animals , Cognition/physiology , Biological Evolution , Mammals , Neurons/physiologyABSTRACT
Migrating birds have developed remarkable navigational capabilities to successfully master biannual journeys between their breeding and wintering grounds. To reach their intended destination, they need to calculate navigational goals from a large variety of natural directional and positional cues to set a meaningful motor output command. One brain area, which has been associated with such executive functions, is the nidopallium caudolaterale (NCL), which, due to its striking similarities in terms of neurochemistry, connectivity and function, is considered analogous to the mammalian prefrontal cortex. To establish a baseline for further analyses elucidating the neuronal correlates underlying avian navigation, we performed quantitative and qualitative analyses of dopaminergic fibres in the brains of long-distance night-migratory Eurasian blackcaps (Sylvia atricapilla). We identified four regions in the caudal telencephalon, each of which was characterized by its specific dopaminergic innervation pattern. At least three of them presumably constitute subareas of the NCL in Eurasian blackcaps and could thus be involved in integrating navigational input from different sensory systems. The observed heterogeneity and parcellation of the NCL subcompartments in this migratory species could be a consequence of the special demands related to navigation.
Subject(s)
Passeriformes , Animals , Brain , Dopamine , Mammals , Passeriformes/physiology , Prefrontal Cortex/physiology , Seasons , TelencephalonABSTRACT
Numerical cognition is ubiquitous in the animal kingdom. Domestic chicks are a widely used developmental model for studying numerical cognition. Soon after hatching, chicks can perform sophisticated numerical tasks. Nevertheless, the neural basis of their numerical abilities has remained unknown. Here, we describe number neurons in the caudal nidopallium (functionally equivalent to the mammalian prefrontal cortex) of young domestic chicks. Number neurons that we found in young chicks showed remarkable similarities to those in the prefrontal cortex and caudal nidopallium of adult animals. Thus, our results suggest that numerosity perception based on number neurons might be an inborn feature of the vertebrate brain.
Subject(s)
Brain , Cognition , Neurons , Perception , Animals , Brain/cytology , Chickens , Neurons/cytologyABSTRACT
The light-dependent magnetic compass sense of night-migratory songbirds can be disrupted by weak radiofrequency fields. This finding supports a quantum mechanical, radical-pair-based mechanism of magnetoreception as observed for isolated cryptochrome 4, a protein found in birds' retinas. The exact identity of the magnetically sensitive radicals in cryptochrome is uncertain in vivo, but their formation seems to require a bound flavin adenine dinucleotide chromophore and a chain of four tryptophan residues within the protein. Resulting from the hyperfine interactions of nuclear spins with the unpaired electrons, the sensitivity of the radicals to radiofrequency magnetic fields depends strongly on the number of magnetic nuclei (hydrogen and nitrogen atoms) they contain. Quantum-chemical calculations suggested that electromagnetic noise in the frequency range 75-85 MHz could give information about the identity of the radicals involved. Here, we show that broadband 75-85 MHz radiofrequency fields prevent a night-migratory songbird from using its magnetic compass in behavioural experiments. These results indicate that at least one of the components of the radical pair involved in the sensory process of avian magnetoreception must contain a substantial number of strong hyperfine interactions as would be the case if a flavin-tryptophan radical pair were the magnetic sensor.
Subject(s)
Songbirds , Taxis Response , Animal Migration , Animals , Cryptochromes/metabolism , Flavins , Magnetic Fields , Songbirds/metabolism , TryptophanABSTRACT
Since the ground-breaking discovery that in-egg light exposure triggers the emergence of visual lateralisation, domestic chicks became a crucial model for research on the interaction of environmental and genetic influences for brain development. In domestic chick embryos, light exposure induces neuroanatomical asymmetries in the strength of visual projections from the thalamus to the visual Wulst. Consequently, the right visual Wulst receives more bilateral information from the two eyes than the left one. How this impacts visual Wulst's physiology is still unknown. This paper investigates the visual response properties of neurons in the left and right Wulst of dark- and light-incubated chicks, studying the effect of light incubation on bilaterally responsive cells that integrate information from both eyes. We recorded from a large number of visually responsive units, providing the first direct evidence of lateralisation in the neural response properties of units of the visual Wulst. While we confirm that some forms of lateralisation are induced by embryonic light exposure, we found also many cases of light-independent asymmetries. Moreover, we found a strong effect of in-egg light exposure on the general development of the functional properties of units in the two hemispheres. This indicates that the effect of embryonic stimulation goes beyond its contribution to the emergence of some forms of lateralisation, with influences on the maturation of visual units in both hemispheres.
Subject(s)
Chickens , Functional Laterality , Animals , Chick Embryo , Neurons , Thalamus , Visual PathwaysABSTRACT
Night-migratory songbirds can use geomagnetic information to navigate over thousands of kilometres with great precision. A crucial part of the magnetic 'map' information used by night-migratory songbirds is conveyed via the ophthalmic branches of the trigeminal nerves to the trigeminal brainstem complex, where magnetic-driven neuronal activation has been observed. However, it is not known how this information reaches the forebrain for further processing. Here, we show that the magnetically activated region in the trigeminal brainstem of migratory Eurasian blackcaps (Sylvia atricapilla) represents a morphologically distinctive neuronal population with an exclusive and previously undescribed projection to the telencephalic frontal nidopallium. This projection is clearly different from the known trigeminal somatosensory pathway that we also confirmed both by neuronal tracing and by a thorough morphometric analysis of projecting neurons. The new pathway we identified here represents part of a brain circuit that-based on the known nidopallial connectivities in birds-could potentially transmit magnetic 'map' information to key multisensory integration centres in the brain known to be critically involved in spatial memory formation, cognition and/or controlling executive behaviour, such as navigation, in birds.
Subject(s)
Animal Migration , Brain/physiology , Songbirds/physiology , Spatial Navigation , Animals , Eye , Magnetic Phenomena , Magnetics , Orientation , Trigeminal NerveABSTRACT
According to the currently prevailing theory, the magnetic compass sense in night-migrating birds relies on a light-dependent radical-pair-based mechanism. It has been shown that radio waves at megahertz frequencies disrupt magnetic orientation in migratory birds, providing evidence for a quantum-mechanical origin of the magnetic compass. Still, many crucial properties, e.g. the lifetime of the proposed magnetically sensitive radical pair, remain unknown. The current study aims to estimate the spin coherence time of the radical pair, based on the behavioural responses of migratory birds to broadband electromagnetic fields covering the frequency band 0.1-100 kHz. A finding that the birds were unable to use their magnetic compass under these conditions would imply surprisingly long-lived (greater than 10 µs) spin coherence. However, we observed no effect of 0.1-100 kHz radiofrequency (RF) fields on the orientation of night-migratory Eurasian blackcaps (Sylvia atricapilla). This suggests that the lifetime of the spin coherence involved in magnetoreception is shorter than the period of the highest frequency RF fields used in this experiment (i.e. approx. 10 µs). This result, in combination with an earlier study showing that 20-450 kHz electromagnetic fields disrupt magnetic compass orientation, suggests that the spin coherence lifetime of the magnetically sensitive radical pair is in the range 2-10 µs.
Subject(s)
Animal Migration , Circadian Rhythm , Noise , Songbirds , Taxis Response , Animals , Electromagnetic Fields , Orientation/physiologyABSTRACT
Recently, virtual magnetic displacement experiments have shown that magnetic cues are indeed important for determining position in migratory birds; but which sensory system(s) do they use to detect the magnetic map cues? Here, we show that Eurasian reed warblers need trigeminal input to detect that they have been virtually magnetically displaced. Birds with bilaterally ablated ophthalmic branches of the trigeminal nerves were not able to re-orient towards their conspecific breeding grounds after a virtual magnetic displacement, exactly like they were not able to compensate for a real physical displacement. In contrast, sham-operated reed warblers re-oriented after the virtual displacement, like intact controls did in the past. Our results show that trigeminally mediated sensory information is necessary for the correct function of the reed warblers' magnetic positioning system.
Subject(s)
Animal Migration , Magnetic Phenomena , Orientation, Spatial , Songbirds/physiology , Trigeminal Nerve/physiology , AnimalsABSTRACT
Long-distance avian migrants, e.g. Eurasian reed warblers (Acrocephalus scirpaceus), can precisely schedule events of their annual cycle. However, the proximate mechanisms controlling annual cycle and their interplay with environmental factors are poorly understood. We artificially interrupted breeding in reed warblers by bringing them into captivity and recording birds' locomotor activity for 5-7 days. Over this time, most of the captive birds gradually developed nocturnal locomotor activity not observed in breeding birds. When the birds were later released and radio-tracked, the individuals with highly developed caged activity performed nocturnal flights. We also found that reed warblers kept indoors without access to local cues developed a higher level of nocturnal activity compared to the birds kept outdoors with an access to the familiar environment. Also, birds translocated from a distant site (21 km) had a higher motivation to fly at night-time after release compared to the birds captured within 1 km of a study site. Our study suggests that an interrupted breeding triggers development of nocturnal locomotor activity in cages, and the level of activity is correlated with motivation to perform nocturnal flights in the wild, which can be restrained by familiar environment.
Subject(s)
Animal Migration , Locomotion , Songbirds/physiology , Animals , Environment , Flight, Animal , Time FactorsABSTRACT
Previously, it has been shown that long-distance migrants, garden warblers (Sylvia borin), were disoriented in the presence of narrow-band oscillating magnetic field (1.403 MHz OMF, 190 nT) during autumn migration. This agrees with the data of previous experiments with European robins (Erithacus rubecula). In this study, we report the results of experiments with garden warblers tested under a 1.403 MHz OMF with various amplitudes (â¼0.4, 1, â¼2.4, 7 and 20 nT). We found that the ability of garden warblers to orient in round arenas using the magnetic compass could be disrupted by a very weak oscillating field, such as an approximate 2.4, 7 and 20 nT OMF, but not by an OMF with an approximate 0.4 nT amplitude. The results of the present study indicate that the sensitivity threshold of the magnetic compass to the OMF lies around 2-3 nT, while in experiments with European robins the birds were disoriented in a 15 nT OMF but could choose the appropriate migratory direction when a 5 nT OMF was added to the stationary magnetic field. The radical-pair model, one of the mainstream theories of avian magnetoreception, cannot explain the sensitivity to such a low-intensity OMF, and therefore, it needs further refinement.
Subject(s)
Animal Migration/physiology , Magnetic Fields , Songbirds/physiology , Taxis Response/physiology , AnimalsABSTRACT
The longitude problem (determining east-west position) is a classical problem in human sea navigation. Prior to the use of GPS satellites, extraordinarily accurate clocks measuring the difference between local time and a fixed reference (e.g., GMT) [1] were needed to determine longitude. Birds do not appear to possess a time-difference clock sense [2]. Nevertheless, experienced night-migratory songbirds can correct for east-west displacements to unknown locations [3-9]. Consequently, migratory birds must solve the longitude problem in a different way, but how they do so has remained a scientific mystery [10]. We suggest that experienced adult Eurasian reed warblers (Acrocephalus scirpaceus) can use magnetic declination to solve the longitude problem at least under some circumstances under clear skies. Experienced migrants tested during autumn migration in Rybachy, Russia, were exposed to an 8.5° change in declination while all other cues remained unchanged. This corresponds to a virtual magnetic displacement to Scotland if and only if magnetic declination is a part of their map. The adult migrants responded by changing their heading by 151° from WSW to ESE, consistent with compensation for the virtual magnetic displacement. Juvenile migrants that had not yet established a navigational map also oriented WSW at the capture site but became randomly oriented when the magnetic declination was shifted 8.5°. In combination with latitudinal cues, which birds are known to detect and use [10-12], magnetic declination could provide the mostly east-west component for a true bi-coordinate navigation system under clear skies for experienced migratory birds in some areas of the globe.
Subject(s)
Animal Migration , Magnetic Fields , Orientation, Spatial , Songbirds/physiology , Animals , Flight, Animal , Russia , ScotlandABSTRACT
It is known that night-migratory songbirds use a magnetic compass measuring the magnetic inclination angle, i.e. the angle between the Earth's surface and the magnetic field lines, but how do such birds orient at the magnetic equator? A previous study reported that birds are completely randomly oriented in a horizontal north-south magnetic field with 0° inclination angle. This seems counter-intuitive, because birds using an inclination compass should be able to separate the north-south axis from the east-west axis, so that bimodal orientation might be expected in a horizontal field. Furthermore, little is known about how shallow inclination angles migratory birds can still use for orientation. In this study, we tested the magnetic compass orientation of night-migratory Eurasian blackcaps (Sylvia atricapilla) in magnetic fields with 5° and 0° inclination. At 5° inclination, the birds oriented as well as they did in the normal 67° inclined field in Oldenburg. In contrast, they were completely randomly oriented in the horizontal field, showing no sign of bimodality. Our results indicate that the inclination limit for the magnetic compass of the blackcap is below 5° and that these birds indeed seem completely unable to use their magnetic compass for orientation in a horizontal magnetic field.
ABSTRACT
Avian malaria parasites (Haemosporida, Plasmodium) are of cosmopolitan distribution, and they have a significant impact on vertebrate host fitness. Experimental studies show that high parasitemia often develops during primary malaria infections. However, field studies only occasionally reveal high parasitemia in free-living birds sampled using the traditional methods of mist-netting or trapping, and light chronic infections predominate. The reason for this discrepancy between field observation and experimental data remains insufficiently understood. Since mist-netting is a passive capture method, two main parameters determine its success in sampling infected birds in wildlife, i. e. the presence of parasitized birds at a study site and their mobility. In other words, the trapping probability depends on the survival rate of birds and their locomotor activity during infection. Here we test (1) the mortality rate of wild birds infected with Plasmodium relictum (the lineage pSGS1), (2) the changes in their behaviour during presence of an aerial predator, and (3) the changes in their locomotor activity at the stage of high primary parasitemia.We show that some behavioural features which might affect a bird's survival during a predator attack (time of reaction, speed of flush flight and take off angle) did not change significantly during primary infection. However, the locomotor activity of infected birds was almost halved compared to control (non-infected) birds during the peak of parasitemia. We report (1) the markedly reduced mobility and (2) the 20% mortality rate caused by P. relictum and conclude that these factors are responsible for the underrepresentation of birds in mist nets and traps during the stage of high primary parasitemia in wildlife. This study indicates that the widespread parasite, P. relictum (pSGS1) influences the behaviour of birds during primary parasitemia. Experimental studies combined with field observations are needed to better understand the mechanisms of pathogenicity of avian malaria parasites and their influence on bird populations.
Subject(s)
Behavior, Animal , Canaries/parasitology , Malaria, Avian/physiopathology , Parasitemia/physiopathology , Animals , Animals, Wild/parasitology , Animals, Wild/physiology , Canaries/physiology , DNA, Protozoan , Flight, Animal , Haemosporida/pathogenicity , Malaria, Avian/parasitology , Parasitemia/parasitology , Plasmodium/pathogenicity , Wings, Animal/parasitology , Wings, Animal/physiopathologyABSTRACT
We report on the experiments on orientation of a migratory songbird, the garden warbler (Sylvia borin), during the autumn migration period on the Courish Spit, Eastern Baltics. Birds in experimental cages, deprived of visual information, showed the seasonally appropriate direction of intended flight with respect to the magnetic meridian. Weak radiofrequency (RF) magnetic field (190 nT at 1.4 MHz) disrupted this orientation ability. These results may be considered as an independent replication of earlier experiments, performed by the group of R. and W. Wiltschko with European robins (Erithacus rubecula). Confirmed outstanding sensitivity of the birds' magnetic compass to RF fields in the lower megahertz range demands for a revision of one of the mainstream theories of magnetoreception, the radical-pair model of birds' magnetic compass.