Noncortical coding of biological motion in newborn chicks' brain.

Biological motion, the typical movement of vertebrates, is perceptually salient for many animal species. Newly hatched domestic chicks and human newborns show a spontaneous preference for simple biological motion stimuli (point-light displays) at birth prior to any visual learning. Despite evidence of such preference at birth, neural studies performed so far have focused on a specialized neural network involving primarily cortical areas. Here, we presented newly hatched visually naïve domestic chicks to either biological or rigid motion stimuli and measured for the first time their brain activation. Immediate Early Gene (c-Fos) expression revealed selective activation in the preoptic area of the hypothalamus and the nucleus taeniae of the amygdala. These results suggest that subpallial/subcortical regions play a crucial role in biological motion perception at hatching, paving the way for future studies on adult animals, including humans.

Responses in the left and right entopallium are differently affected by light stimulation in embryo.

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.

Hierarchical processing of feature, egocentric and relational information for spatial orientation in domestic chicks.

Animals can use different types of information for navigation. Domestic chicks (Gallus gallus) prefer to use local features as a beacon over spatial relational information. However, the role of egocentric navigation strategies is less understood. Here, we tested domestic chicks' egocentric and allocentric orientation abilities in a large circular arena. In experiment 1, we investigated whether domestic chicks possess a side bias during viewpoint-dependent egocentric orientation, revealing facilitation for targets on the chicks' left side. Experiment 2 showed that local features are preferred over viewpoint-dependent egocentric information when the two conflict. Lastly, in experiment 3, we found that in a situation where there is a choice between egocentric and allocentric spatial relational information provided by free-standing objects, chicks preferentially rely on egocentric information. We conclude that chicks orient according to a hierarchy of cues, in which the use of the visual appearance of an object is the dominant strategy, followed by viewpoint-dependent egocentric information and finally by spatial relational information.

Spatial cognition and the avian hippocampus: Research in domestic chicks.

In this review, we discuss the functional equivalence of the avian and mammalian hippocampus, based mostly on our own research in domestic chicks, which provide an important developmental model (most research on spatial cognition in other birds relies on adult animals). In birds, like in mammals, the hippocampus plays a central role in processing spatial information. However, the structure of this homolog area shows remarkable differences between birds and mammals. To understand the evolutionary origin of the neural mechanisms for spatial navigation, it is important to test how far theories developed for the mammalian hippocampus can also be applied to the avian hippocampal formation. To address this issue, we present a brief overview of studies carried out in domestic chicks, investigating the direct involvement of chicks' hippocampus homolog in spatial navigation.

Active exploration of an environment drives the activation of the hippocampus-amygdala complex of domestic chicks.

In birds, like in mammals, the hippocampus critically mediates spatial navigation through the formation of a spatial map. This study investigates the impact of active exploration of an environment on the hippocampus of young domestic chicks. Chicks that were free to actively explore the environment exhibited a significantly higher neural activation (measured by c-Fos expression) compared with those that passively observed the same environment from a restricted area. The difference was limited to the anterior and the dorsolateral parts of the intermediate hippocampus. Furthermore, the nucleus taeniae of the amygdala showed a higher c-Fos expression in the active exploration group than in the passive observation group. In both brain regions, brain activation was correlated with the number of locations that chicks visited during the test. This suggests that the increase of c-Fos expression in the hippocampus is related to increased firing rates of spatially coding neurons. Furthermore, our study indicates a functional linkage of the hippocampus and nucleus taeniae of the amygdala in processing spatial information. Overall, with the present study, we confirm that in birds, like in mammals, hippocampus and amygdala functions are linked and likely related to spatial representations.

The Geometric World of Fishes: A Synthesis on Spatial Reorientation in Teleosts.

Fishes navigate through underwater environments with remarkable spatial precision and memory. Freshwater and seawater species make use of several orientation strategies for adaptative behavior that is on par with terrestrial organisms, and research on cognitive mapping and landmark use in fish have shown that relational and associative spatial learning guide goal-directed navigation not only in terrestrial but also in aquatic habitats. In the past thirty years, researchers explored spatial cognition in fishes in relation to the use of environmental geometry, perhaps because of the scientific value to compare them with land-dwelling animals. Geometric navigation involves the encoding of macrostructural characteristics of space, which are based on the Euclidean concepts of "points", "surfaces", and "boundaries". The current review aims to inspect the extant literature on navigation by geometry in fishes, emphasizing both the recruitment of visual/extra-visual strategies and the nature of the behavioral task on orientation performance.

Anatomical asymmetries in the tectofugal pathway of dark-incubated domestic chicks: Rightwards lateralization of parvalbumin neurons in the entopallium.

The discovery of the role of light exposure for the development of lateralization in domestic chick embryos revolutionized this research field. However, two main issues remain unresolved: (i) while in chicks anatomical light-dependent lateralization is mostly confined to the thalamofugal visual pathway, in pigeons only the tectofugal pathway is lateralized after light exposure. However, no study in either species ever investigated anatomical lateralization in the entopallium, the forebrain station of the tectofugal pathway. (ii) It is now known that lateralization can be observed also in dark-incubated chicks, both at the behavioural and at the Immediate Early Gene-expression level. We hypothesized that lateralization of the tectofugal system may underlie these light-independent effects. To investigate structural lateralization in the tectofugal pathway of dark-incubated chicks, we used parvalbumin (PV) as a marker of a sub population of entopallial neurons, quantifying PV-ir cell densities in the left and right entopallium. We found higher density in the right hemisphere, revealing for the first time anatomical lateralization in entopallium and confirming its potential role in supporting lateralized brain processing in dark-incubated birds. Results are discussed in relation to the possible functional role of PV-ir cells in inhibitory neural functions.

Selective activation of the right hippocampus during navigation by spatial cues in domestic chicks (Gallus gallus).

In different vertebrate species, hippocampus plays a crucial role for spatial orientation. However, even though cognitive lateralization is widespread in the animal kingdom, the lateralization of this hippocampal function has been poorly studied. The aim of the present study was to investigate the lateralization of hippocampal activation in domestic chicks, during spatial navigation in relation to free-standing objects. Two groups of chicks were trained to find food in one of the feeders located in a large circular arena. Chicks of one group solved the task using the relational spatial information provided by free-standing objects present in the arena, while the other group used the local appearance of the baited feeder as a beacon. The immediate early gene product c-Fos was employed to map neural activation of hippocampus and medial striatum of both hemispheres. Chicks that used spatial cues for navigation showed higher activation of the right hippocampus compared to chicks that oriented by local features and compared to the left hippocampus. Such differences between the two groups were not present in the left hippocampus or in the medial striatum. Relational spatial information seems thus to be selectively processed by the right hippocampus in domestic chicks. The results are discussed in light of existing evidence of hippocampal lateralization of spatial processing in chicks, with particular attention to the contrasting evidence found in pigeons.

Neural basis of unfamiliar conspecific recognition in domestic chicks (Gallus Gallus domesticus).

Domestic chickens are able to distinguish familiar from unfamiliar conspecifics, however the neuronal mechanisms mediating this behaviour are almost unknown. Moreover, the lateralisation of chicks' social recognition has only been investigated at the behavioural level, but not at the neural level. The aim of the present study was to test the hypothesis that exposure to unfamiliar conspecifics will selectively activate septum, hippocampus or nucleus taeniae of the amygdala of young domestic chicks. Moreover we also wanted to test the lateralisation of this response. For this purpose, we used the immediate early gene product c-Fos to map neural activity. Chicks were housed in pairs for one week. At test, either one of the two chicks was exchanged by an unfamiliar individual (experimental 'unfamiliar' group) or the familiar individual was briefly removed and then placed back in its original cage (control 'familiar' group). Analyses of chicks' interactions with the familiar/unfamiliar social companion revealed a higher number of social pecks directed towards unfamiliar individuals, compared to familiar controls. Moreover, in the group exposed to the unfamiliar individual a significantly higher activation was present in the dorsal and ventral septum of the left hemisphere and in the ventral hippocampus of the right hemisphere, compared to the control condition. These effects were neither present in other subareas of hippocampus or septum, nor in the nucleus taeniae of the amygdala. Our study thus indicates selective lateralised involvement of domestic chicks' septal and hippocampal subregions in responses to unfamiliar conspecific.

The effect of monocular occlusion on hippocampal c-Fos expression in domestic chicks (Gallus gallus).

In birds, like in mammals, the hippocampus is particularly sensitive to exposure to novel environments, a function that is based on visual input. Chicks' eyes are placed laterally and their optic fibers project mainly to the contralateral brain hemispheres, with only little direct interhemispheric coupling. Thus, monocular occlusion has been frequently used in chicks to document functional specialization of the two hemispheres. However, we do not know whether monocular occlusion influences hippocampal activation. The aim of the present work was to fill this gap by directly testing this hypothesis. To induce hippocampal activation, chicks were exposed to a novel environment with their left or right eye occluded, or in conditions of binocular vision. Their hippocampal expression of c-Fos (neural activity marker) was compared to a baseline group that remained in a familiar environment. Interestingly, while the hippocampal activation in the two monocular groups was not different from the baseline, it was significantly higher in the binocular group exposed to the novel environment. This suggest that the representation of environmental novelty in the hippocampus of domestic chicks involves strong binocular integration.

The use of spatial and local cues for orientation in domestic chicks (Gallus gallus).

Birds have been widely used to study spatial orientation. However, since different birds rely on different types of visual information to find goal locations (such as spatial information from free-standing objects or local cues, i.e. characteristics of a goal location like color and shape), it is important to investigate this aspect in each model species. The aim of the present study was to clarify whether domestic chicks, a ground-living bird and a widely used model for the comparative study of spatial orientation, are able to reorient in relation to free-standing objects and if they preferentially follow local or spatial cues. Furthermore, we also investigated whether monocular eye occlusion influences the ability of chicks to use spatial or local cues. Chicks were trained and tested in a large circular arena with free-standing objects providing relational spatial information, to find food in one of the feeders. We found that dark-incubated male chicks were able to reorient in relation to distinct, free-standing landmarks (Experiment 1), but when local and spatial cues were put in conflict, chicks significantly preferred local cues over spatial cues (Experiment 3). Moreover, while the use of one eye system only was not sufficient to orient by spatial cues (Experiment 2), the preference for local over spatial cues was independent of monocular occlusion (Experiment 4). The results are discussed in relation to our general knowledge of spatial information processing in domestic chicks.

Spontaneous and light-induced lateralization of immediate early genes expression in domestic chicks.

Exposure of domestic chicks' eggs to light during embryo incubation stimulates asymmetrically the two eye-systems, reaching selectively the right eye (left hemisphere) and inducing asymmetries at the behavioral and neural level. Surprisingly, though, some types of lateralization have been observed also in dark incubated chicks, especially at the behavioral level. Here we investigate the mechanisms subtending the development of lateralization, in the presence and in the absence of embryonic light exposure. We measured the baseline level of expression for the immediate early gene product c-Fos, used as an indicator of the spontaneous level of neural activity and plasticity in four areas of the two hemispheres (preoptic area, septum, hippocampus and intermediate medial mesopallium). Additional DAPI staining measured overall cell density (regardless of c-Fos expression), ruling out any confound due to underlying asymmetries in cell density between the hemispheres. In different brain areas, c-Fos expression was lateralized either in light- (septum) or in dark-incubated chicks (preoptic area). Light exposure increased c-Fos expression in the left hemisphere, suggesting that c-Fos expression could participate to the known effects of light stimulation on brain asymmetries. Interestingly, this effect was visible few days after the end of the light exposure, revealing a delayed effect of light exposure on c-Fos baseline expression in brain areas outside the visual pathways. In the preoptic area of dark incubated chicks, we found a rightward bias for c-Fos expression, revealing that lateralization of the baseline level of activity and plasticity is present in the developing brain also in the absence of light exposure.