Audio-Visual Interference During Motion Discrimination in Starlings.

Motion discrimination is essential for animals to avoid collisions, to escape from predators, to catch prey or to communicate. Although most terrestrial vertebrates can benefit by combining concurrent stimuli from sound and vision to obtain a most salient percept of the moving object, there is little research on the mechanisms involved in such cross-modal motion discrimination. We used European starlings as a model with a well-studied visual and auditory system. In a behavioural motion discrimination task with visual and acoustic stimuli, we investigated the effects of cross-modal interference and attentional processes. Our results showed an impairment of motion discrimination when the visual and acoustic stimuli moved in opposite directions as compared to congruent motion direction. By presenting an acoustic stimulus of very short duration, thus lacking directional motion information, an additional alerting effect of the acoustic stimulus became evident. Finally, we show that a temporally leading acoustic stimulus did not improve the response behaviour compared to the synchronous presentation of the stimuli as would have been expected in case of major alerting effects. This further supports the importance of congruency and synchronicity in the current test paradigm with a minor role of attentional processes elicited by the acoustic stimulus. Together, our data clearly show cross-modal interference effects in an audio-visual motion discrimination paradigm when carefully selecting real-life stimuli under parameter conditions that meet the known criteria for cross-modal binding.

Violation of the Unity Assumption Disrupts Temporal Ventriloquism Effect in Starlings.

When stimuli from different sensory modalities are received, they may be combined by the brain to form a multisensory percept. One key mechanism for multisensory binding is the unity assumption under which multisensory stimuli that share certain physical properties like temporal and/or spatial correspondence are grouped together as deriving from one object. In humans, evidence for a role of the unity assumption has been found in spatial tasks and also in temporal tasks using stimuli that share physical properties (speech-related stimuli, musical and synesthetically congruent stimuli). In our study, we investigate the role of the unity assumption in an animal model in a temporal order judgment task. When subjects are asked to indicate which of two spatially separated visual stimuli appeared first in time, performance improves when the visual stimuli are paired (in time) with spatially non-informative acoustic cues, a phenomenon known as the temporal ventriloquism effect. Here, we show that European starlings perform better when one singleton acoustic cue is paired with the first visual stimulus as compared to pairing with the second visual stimulus. This shows, in combination with our previous study, that a non-informative singleton acoustic cue, when temporally paired with the first visual stimulus, triggers alerting while, when temporally pairing with the second visual stimulus, it prevents a temporal ventriloquism effect because the unity assumption is violated. Thus, the unity assumption influences sensory perception not only in humans but also in an animal model. The importance of the unity assumption in this task supports the idea that the temporal ventriloquism effect, similar to the spatial ventriloquism effect, is based on multisensory binding and integration but not on alerting effects.

Temporal ventriloquism effect in European starlings: Evidence for two parallel processing pathways.

The brain constantly has to interpret stimuli from a range of modalities originating from the same or different objects to create unambiguous percepts. The mechanisms of such multisensory processing have been intensely studied with respect to the time window of integration or the effect of spatial separation. However, the neural mechanisms remain elusive with respect to the role of alerting effects and multisensory integration. We addressed this issue by choosing a test paradigm where we could manipulate potentially alerting stimuli and simultaneously activating stimuli independently: We measured the temporal ventriloquism effect in European starlings by using the temporal order judgment paradigm with subjects judging the temporal order of the lighting of 2 spatially separated lights. If spatially noninformative acoustic stimuli were added to the visual stimuli the performance improved when the 2 visual stimuli were flanked by acoustic cues with a small time-offset compared to synchronous presentation. Two acoustic cues presented with asymmetric offsets showed that this effect was mainly driven by the cue trailing the second visual stimulus, while an acoustic cue leading the first visual stimulus had less effect. In contrast, 1 singleton acoustic cue prior to the first visual stimulus, without a second acoustic cue, enhanced performance. Our results support the hypothesis that the first stimulus pair with the leading sound activates alerting mechanisms and enhances neural processing, while the second stimulus pair with the trailing sound drives multisensory integration by simultaneous activation within the temporal binding window. (PsycINFO Database Record

Hand rearing affects emotional responses but not basic cognitive performance in European starlings.

Hand rearing is a common procedure in behavioural research on birds. While likely to produce tamer experimental animals, there is a risk that it could induce pathological changes in brain and behaviour similar to those seen in mammals that have experienced maternal separation. We explored the effects of hand rearing on the cognitive and behavioural development of European starlings, Sturnus vulgaris, to assess the generality of results obtained from hand-reared animals. Two groups of age-matched birds were created from the same wild population: one hand-reared from 10 days posthatch and one brought into the laboratory as independent juveniles. These groups were compared on a battery of neuropsychological tasks designed to probe different aspects of cognitive function including learning, perseverative cognition, interval timing, neophobia and impulsivity. There was no evidence for cognitive impairment in the hand-reared birds. They did not have reduced learning speed, impairments in accuracy or precision of interval timing or pathological perseverative cognition compared to the wild-caught birds. Additionally, there was no evidence that birds that developed stereotypies in laboratory cages (predominantly the wild-caught birds) had any cognitive impairments, although this may be because no birds had severe, crystallized stereotypies. There was some evidence that hand-reared birds were less neophobic and less impulsive than wild-caught birds, suggesting that hand rearing might alter emotionally mediated decision making in a direction usually associated with reduced developmental stress in mammals. This study therefore supports the use of hand rearing as an experimental procedure in behavioural research on passerine birds.

Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns.

Based on quantitative cluster analyses of 52 constitutively expressed or behaviorally regulated genes in 23 brain regions, we present a global view of telencephalic organization of birds. The patterns of constitutively expressed genes revealed a partial mirror image organization of three major cell populations that wrap above, around, and below the ventricle and adjacent lamina through the mesopallium. The patterns of behaviorally regulated genes revealed functional columns of activation across boundaries of these cell populations, reminiscent of columns through layers of the mammalian cortex. The avian functionally regulated columns were of two types: those above the ventricle and associated mesopallial lamina, formed by our revised dorsal mesopallium, hyperpallium, and intercalated hyperpallium; and those below the ventricle, formed by our revised ventral mesopallium, nidopallium, and intercalated nidopallium. Based on these findings and known connectivity, we propose that the avian pallium has four major cell populations similar to those in mammalian cortex and some parts of the amygdala: 1) a primary sensory input population (intercalated pallium); 2) a secondary intrapallial population (nidopallium/hyperpallium); 3) a tertiary intrapallial population (mesopallium); and 4) a quaternary output population (the arcopallium). Each population contributes portions to columns that control different sensory or motor systems. We suggest that this organization of cell groups forms by expansion of contiguous developmental cell domains that wrap around the lateral ventricle and its extension through the middle of the mesopallium. We believe that the position of the lateral ventricle and its associated mesopallium lamina has resulted in a conceptual barrier to recognizing related cell groups across its border, thereby confounding our understanding of homologies with mammals.

The development of stereotypic behavior in caged European starlings, Sturnus vulgaris.

Stereotypic behavior in captive animals has been hypothesized to emerge from thwarted natural behavior patterns and is thought to be more common in captive-reared animals. However, data on the early stages of developing stereotypies are currently scarce. We compared the development of stereotypic route-tracing and somersaulting in hand-reared and wild-caught starlings placed in individual cages for the first time. We found that wild-caught birds were less active but showed more escape motivation and more evidence of route-tracing behavior. Furthermore, somersaulting was only observed in wild-caught birds. Development of somersaulting was predicted by subtle differences in behavior during the first few days in cages and developed in individuals with low levels of route-tracing behavior. Our data suggest a role for escape motivation in the development of starling stereotypies and additionally that route-tracing and somersaulting may represent alternative outlets for thwarted escape. In contrast to observations from mammals, our results show that stereotypies are more common in wild-caught starlings.

Fear and exploration in European starlings (Sturnus vulgaris): a comparison of hand-reared and wild-caught birds.

The revision of EU legislation will ban the use of wild-caught animals in scientific procedures. This change is partially predicated on the assumption that captive-rearing produces animals with reduced fearfulness. Previously, we have shown that hand-reared starlings (Sturnus vulgaris) indeed exhibit reduced fear of humans compared to wild-caught conspecifics. Here, we asked whether this reduction in fear in hand-reared birds is limited to fear of humans or extends more generally to fear of novel environments and novel objects. Comparing 6-8 month old birds hand-reared in the lab with age-matched birds caught from the wild as fledged juveniles a minimum of 1 month previously, we examined the birds' initial reactions in a novel environment (a small cage) and found that wild-caught starlings were faster to initiate movement compared to the hand-reared birds. We interpret this difference as evidence for greater escape motivation in the wild-caught birds. In contrast, we found no differences between hand-reared and wild-caught birds when tested in novel object tests assumed to measure neophobia and exploratory behaviour. Moreover, we found no correlations between individual bird's responses in the different tests, supporting the idea that these measure different traits (e.g. fear and exploration). In summary, our data show that developmental origin affects one measure of response to novelty in young starlings, indicative of a difference in either fear or coping style in a stressful situation. Our data contribute to a growing literature demonstrating effects of early-life experience on later behaviour in a range of species. However, since we did not find consistent evidence for reduced fearfulness in hand-reared birds, we remain agnostic about the welfare benefits of hand-rearing as a method for sourcing wild birds for behavioural and physiological research.

Hand-rearing reduces fear of humans in European starlings, Sturnus vulgaris.

Pending changes in European legislation ban the use of wild-caught animals in research. This change is partly justified on the assumption that captive-breeding (or hand-rearing) increases welfare of captive animals because these practices result in animals with reduced fear of humans. However, there are few actual data on the long-term behavioural effects of captive-breeding in non-domestic species, and these are urgently needed in order to understand the welfare and scientific consequences of adopting this practice. We compared the response of hand-reared and wild-caught starlings to the presence of a human in the laboratory. During human presence, all birds increased their general locomotor activity but the wild-caught birds moved away from the human and were less active than the hand-reared birds. After the human departed, the wild-caught birds were slower to decrease their activity back towards baseline levels, and showed a dramatic increase in time at the periphery of the cage compared with the hand-reared birds. We interpret these data as showing evidence of a greater fear response in wild-caught birds with initial withdrawal followed by a subsequent rebound of prolonged attempts to escape the cage. We found no effects of environmental enrichment. However, birds in cages on low shelves were less active than birds on upper shelves, and showed a greater increase in the time spent at the periphery of their cages after the human departed, perhaps indicating that the lower cages were more stressful. In demonstrating reduced fear of humans in hand-reared birds, our results support one of the proposed welfare benefits of this practice, but without further data on the possible welfare costs of hand-rearing, it is not yet possible to reach a general conclusion about its net welfare impact. However, our results confirm a clear scientific impact of both hand-rearing and cage position at the behavioural level.

Magpies can use local cues to retrieve their food caches.

Much importance has been placed on the use of spatial cues by food-hoarding birds in the retrieval of their caches. In this study, we investigate whether food-hoarding birds can be trained to use local cues ("beacons") in their cache retrieval. We test magpies (Pica pica) in an active hoarding-retrieval paradigm, where local cues are always reliable, while spatial cues are not. Our results show that the birds use the local cues to retrieve their caches, even when occasionally contradicting spatial information is available. The design of our study does not allow us to test rigorously whether the birds prefer using local over spatial cues, nor to investigate the process through which they learn to use local cues. We furthermore provide evidence that magpies develop landmark preferences, which improve their retrieval accuracy. Our findings support the hypothesis that birds are flexible in their use of memory information, using a combination of the most reliable or salient information to retrieve their caches.

The use of passerine bird species in laboratory research: implications of basic biology for husbandry and welfare.

Passerine birds are important models in fundamental biological research, with as many as 300,000 individuals used in laboratory experiments worldwide annually. However, because the use of passerines is rare compared with that of more conventional laboratory animals, there is often a lack of information about the basic biology and husbandry requirements of these species. We aim to address this deficit by providing an overview of the most salient aspects of passerine biology and their implications for laboratory husbandry and welfare. We start by describing the characteristics that make these birds useful and interesting research subjects. Specifically, we highlight features (e.g., birdsong) of passerine biology that differentiate these birds from more common laboratory animals. Next, we consider the implications of passerine biology for husbandry in the laboratory. Many of the aspects of passerine biology that make these species valuable to scientists are also likely to be affected by environmental variables; a good knowledge of these variables is necessary in order to choose appropriate laboratory conditions for passerines. We outline how the developmental history of the birds and choices of caging, feeding, and environmental regimes might influence their physiology and behavior and thus affect both the welfare of the birds and the quality of the resulting data. We stress the importance of a sound understanding of the biology of any species to ensure good welfare and good science.

Quantification of abnormal repetitive behaviour in captive European starlings (Sturnus vulgaris).

Stereotypies are repetitive, unvarying and goalless behaviour patterns that are often considered indicative of poor welfare in captive animals. Quantifying stereotypies can be difficult, particularly during the early stages of their development when behaviour is still flexible. We compared two methods for objectively quantifying the development of route-tracing stereotypies in caged starlings. We used Markov chains and T-pattern analysis (implemented by the software package, Theme) to identify patterns in the sequence of locations a bird occupied within its cage. Pattern metrics produced by both methods correlated with the frequency of established measures of stereotypic behaviour and abnormal behaviour patterns counted from video recordings, suggesting that both methods could be useful for identifying stereotypic individuals and quantifying stereotypic behaviour. We discuss the relative benefits and disadvantages of the two approaches.

Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin.

Vocal learning is a critical behavioral substrate for spoken human language. It is a rare trait found in three distantly related groups of birds-songbirds, hummingbirds, and parrots. These avian groups have remarkably similar systems of cerebral vocal nuclei for the control of learned vocalizations that are not found in their more closely related vocal non-learning relatives. These findings led to the hypothesis that brain pathways for vocal learning in different groups evolved independently from a common ancestor but under pre-existing constraints. Here, we suggest one constraint, a pre-existing system for movement control. Using behavioral molecular mapping, we discovered that in songbirds, parrots, and hummingbirds, all cerebral vocal learning nuclei are adjacent to discrete brain areas active during limb and body movements. Similar to the relationships between vocal nuclei activation and singing, activation in the adjacent areas correlated with the amount of movement performed and was independent of auditory and visual input. These same movement-associated brain areas were also present in female songbirds that do not learn vocalizations and have atrophied cerebral vocal nuclei, and in ring doves that are vocal non-learners and do not have cerebral vocal nuclei. A compilation of previous neural tracing experiments in songbirds suggests that the movement-associated areas are connected in a network that is in parallel with the adjacent vocal learning system. This study is the first global mapping that we are aware for movement-associated areas of the avian cerebrum and it indicates that brain systems that control vocal learning in distantly related birds are directly adjacent to brain systems involved in movement control. Based upon these findings, we propose a motor theory for the origin of vocal learning, this being that the brain areas specialized for vocal learning in vocal learners evolved as a specialization of a pre-existing motor pathway that controls movement.

Lateralized activation of Cluster N in the brains of migratory songbirds.

Cluster N is a cluster of forebrain regions found in night-migratory songbirds that shows high activation of activity-dependent gene expression during night-time vision. We have suggested that Cluster N may function as a specialized night-vision area in night-migratory birds and that it may be involved in processing light-mediated magnetic compass information. Here, we investigated these ideas. We found a significant lateralized dominance of Cluster N activation in the right hemisphere of European robins (Erithacus rubecula). Activation predominantly originated from the contralateral (left) eye. Garden warblers (Sylvia borin) tested under different magnetic field conditions and under monochromatic red light did not show significant differences in Cluster N activation. In the fairly sedentary Sardinian warbler (Sylvia melanocephala), which belongs to the same phyolgenetic clade, Cluster N showed prominent activation levels, similar to that observed in garden warblers and European robins. Thus, it seems that Cluster N activation occurs at night in all species within predominantly migratory groups of birds, probably because such birds have the capability of switching between migratory and sedentary life styles. The activation studies suggest that although Cluster N is lateralized, as is the dependence on magnetic compass orientation, either Cluster N is not involved in magnetic processing or the magnetic modulations of the primary visual signal, forming the basis for the currently supported light-dependent magnetic compass mechanism, are relatively small such that activity-dependent gene expression changes are not sensitive enough to pick them up.

Night-vision brain area in migratory songbirds.

Twice each year, millions of night-migratory songbirds migrate thousands of kilometers. To find their way, they must process and integrate spatiotemporal information from a variety of cues including the Earth's magnetic field and the night-time starry sky. By using sensory-driven gene expression, we discovered that night-migratory songbirds possess a tight cluster of brain regions highly active only during night vision. This cluster, here named "cluster N," is located at the dorsal surface of the brain and is adjacent to a known visual pathway. In contrast, neuronal activation of cluster N was not increased in nonmigratory birds during the night, and it disappeared in migrants when both eyes were covered. We suggest that in night-migratory songbirds cluster N is involved in enhanced night vision, and that it could be integrating vision-mediated magnetic and/or star compass information for night-time navigation. Our findings thus represent an anatomical and functional demonstration of a specific night-vision brain area.

Migratory birds use head scans to detect the direction of the earth's magnetic field.

Night-migratory songbirds are known to use a magnetic compass , but how do they detect the reference direction provided by the geomagnetic field, and where is the sensory organ located? The most prominent characteristic of geomagnetic sensory input, whether based on visual patterns or magnetite-mediated forces , is the predicted symmetry around the north-south or east-west magnetic axis. Here, we show that caged migratory garden warblers perform head-scanning behavior well suited to detect this magnetic symmetry plane. In the natural geomagnetic field, birds move toward their migratory direction after head scanning. In a zero-magnetic field , where no symmetry plane exists, the birds almost triple their head-scanning frequency, and the movement direction after a head scan becomes random. Thus, the magnetic sensory organ is located in the bird's head, and head scans are used to locate the reference direction provided by the geomagnetic field.

Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation.

Migratory birds can use a magnetic compass for orientation during their migratory journeys covering thousands of kilometers. But how do they sense the reference direction provided by the Earth's magnetic field? Behavioral evidence and theoretical considerations have suggested that radical-pair processes in differently oriented, light-sensitive molecules of the retina could enable migratory birds to perceive the magnetic field as visual patterns. The cryptochromes (CRYs) have been suggested as the most likely candidate class of molecules, but do CRYs exist in the retina of migratory birds? Here, we show that at least one CRY1 and one CRY2 exist in the retina of migratory garden warblers and that garden-warbler CRY1 (gwCRY1) is cytosolic. We also show that gwCRY1 is concentrated in specific cells, particularly in ganglion cells and in large displaced ganglion cells, which also showed high levels of neuronal activity at night, when our garden warblers performed magnetic orientation. In addition, there seem to be striking differences in CRY1 expression between migratory and nonmigratory songbirds at night. The difference in CRY1 expression between migrants and nonmigrants is particularly pronounced in the large displaced ganglion cells known to project exclusively to a brain area where magnetically sensitive neurons have been reported. Consequently, cytosolic gwCRY1 is well placed to possibly be the primary magnetic-sensory molecule required for light-mediated magnetoreception.