Uwe Mayer

Spatial memory and the avian hippocampus: Research in zebra finches ☆

The aim of the present review is to show that spatial learning and memory is not a specialty of just a few avian species, and to describe the role of the avian hippocampus in spatial learning, memory and orientation. Based on our own research in zebra finches, we try to give an (not complete and probably biased) overview of this topic, and we also discuss the question of functional equivalence of hippocampus in birds and in mammals in that we question how far theories developed for mammalian hippocampus can also be applied to the avian hippocampal formation.

Brain activation pattern depends on the strategy chosen by zebra finches to solve an orientation task.

SUMMARY Zebra finches (Taeniopygia guttata) were trained to find food in one of four feeders on the floor of an aviary. This feeder was always in the same place during training and was additionally marked by a distinct pattern. In the test trial the distinctly patterned feeder was interchanged with one of the other feeders, so that the birds had to decide to use either the pattern or the original location for finding food. Half of the birds used one strategy and half used the other. According to the strategy applied, different brain areas were activated, as demonstrated by c-Fos immunohistochemistry. The hippocampus was activated when spatial cues were used, while in birds orienting using the pattern of the feeder, part of the collothalamic (tectofugal) visual system showed stronger activation. The visual wulst of the lemnothalamic (thalamofugal) visual system was activated with both strategies, indicating an involvement in both spatial and pattern-directed orientation. Because the experimental situation was the same for all zebra finches, the activation pattern was only dependent on the strategy that was voluntarily chosen by each of the birds.

Filial responses as predisposed and learned preferences: Early attachment in chicks and babies

HighlightsPredispositions orient newborn babies and chicks towards animate objects.Subcortical/subpallial structures may be sufficient to support social predispositions.Social Behaviour Network areas might be involved in unlearnt social behaviours.Hormones facilitate preferences for predisposed stimuli and social attachment.Social predispositions are impaired in newborns at high genetic risk for autism. Abstract To what extent are filial responses the outcome of spontaneous or acquired preferences? The case of domestic chicks illustrates the connection between predisposed and learned knowledge in early social responses. In the absence of specific experience, chicks prefer to approach objects that are more similar to natural social partners (e.g. they prefer face‐like configurations, biological motion, self‐propelled objects and those that move at variable speed). Spontaneous preferences are complemented by filial imprinting, a powerful learning mechanism that enables chicks to quickly learn the features of specific social partners. While neurobiological studies have clarified that the substrates of spontaneous and learned preferences are at least partially distinct in chicks, evidence shows that spontaneous preferences might orient and facilitate imprinting on animate stimuli, such as the mother hen, and that hormones facilitate and strengthen preferences for predisposed stimuli. Preferences towards animate stimuli are observed in human neonates as well. The remarkable consistency between the perceptual cues attended to by newborn babies and naïve chicks suggests that the attentional biases observed in babies are unlikely to result from very rapid post‐natal learning, and confirms that research on precocial species can inform and guide human infant research with regards to both typical and atypical development. This has potentially important biomedical implications, opening new possibilities for the early detection of subjects at risk for autism spectrum disorders. We show how the parallel investigation of predispositions in naïve chicks and human infants, both benefiting from contact with social partners since the beginning of life, has greatly improved our understanding of early responses to social stimuli at the behavioural and neurobiological level.

Visual Wulst analyses where and entopallium analyses what in the zebra finch visual system

Quite a lot of studies have tried to elucidate the differences in function of the two telencephalic targets of the avian visual system. We have tried to find out how the two systems are involved in orientation towards a food tray which is either marked by a special pattern or has to be identified by its relation to spatial cues. In this report, we compared in the zebra finch the effects of Wulst lesions on pattern discrimination with Wulst lesion effects on spatial discrimination, and we examined the effect of entopallium lesions on spatial discrimination. Birds with Wulst lesions showed deficits in spatial discrimination, but not in pattern discrimination. Entopallial lesions caused no deficits in spatial discrimination tasks. Combining the present results with a previous study revealing an impairment of pattern discrimination by such entopallial lesions [19], we are able to demonstrate a double dissociation: namely, an impairment of pattern discrimination by entopallial lesions and impairment of spatial discrimination by Wulst lesions, but no effects of the opposite pairing of task and lesion site. The entopallium is thus involved if the food source is identified by a pattern, and the Wulst if it has to be found by spatial cues.

Hippocampus and medial striatum dissociation during goal navigation by geometry or features in the domestic chick: An immediate early gene study

We employed a standard reference memory task to study the involvement of the hippocampal formation (HF) of domestic chicks that used the boundary geometry of a test environment to orient to and locate a reward. Using the immediate early gene product c‐Fos as a neuronal activity marker, we found enhanced HF activation in chicks that learned to locate rewarded corners using the shape of a rectangular arena compared to chicks trained to solve the task by discriminating local features in a square‐shaped arena. We also analyzed neuronal activity in the medial part of the medial striatum (mMSt). Surprisingly, in mMSt we observed a reverse pattern, with higher activity in the chicks that were trained to locate the goal by local features. Our results identify two seemingly parallel, memory systems in chicks, with HF central to the processing of spatial‐geometrical information and mMSt important in supporting local feature discrimination.

Dynamic features of animate motion activate septal and preoptic areas in visually naïve chicks (Gallus gallus)

The septum is an evolutionarily well-conserved part of the limbic system. It is known to be involved in many aspects of social behavior and is considered a key node of the social behavior network, together with the preoptic area. Involvement of these two brain regions has been recently observed in newly hatched chicks exposed to the natural motion of a living conspecific. However, it is unknown whether these areas respond also to simple motion cues that elicit animacy perception in humans and social predispositions in chicks. For example, naïve chicks are attracted by visual objects that appear to spontaneously change their speed (an index of self-propulsion, typical of animate creatures). Here we show that the right septum and the preoptic area of newly hatched visually naïve chicks exposed to speed changes have higher neuronal activity (revealed by c-Fos expression), compared with that of chicks exposed to constant motion. We thus found an involvement of these two areas in the perception of motion cues associated with animacy in newly hatched chicks without any previous visual experience. This demonstrates their early involvement in processing simple motion cues that allow the detection of animate creatures and elicit social predispositions in this animal model, as well as preferential attention in human infants and the perception of animacy in human adults.

The motion of a living conspecific activates septal and preoptic areas in naive domestic chicks (Gallus gallus)

Predispositions to attend to animate objects are ubiquitous in newborn vertebrates, but little is known about their neural bases. In this study, we wanted to know if exposure to the motion of a living, behaving conspecific will selectively activate septal, preoptic and amygdaloid areas in visually naive domestic chicks. For this purpose, newly hatched chicks were exposed to a live conspecific, whose natural motion presents of course several features typical of animate motion to which chicks are known to be sensitive. In the control group, chicks were exposed to a rotating stuffed chick that showed rigid non‐biological motion. The two stimuli were visually matched with regard to their static features. We measured brain activity by visualizing the immediate early gene product c‐Fos with a standard immunohistochemical procedure. Notably, dorsal right septum and left preoptic area showed higher activation in experimental subjects compared to the control animals. This is, to the best of our knowledge, the first demonstration of septal and preoptic areas involvement in response to the animate motion of a social partner, as opposed to rigid motion of a similarly looking stimulus. Moreover, these results indicate that previous visual experience and specific learning events are not necessary to establish the septal and preoptic areas function, which is present shortly after birth.

First exposure to an alive conspecific activates septal and amygdaloid nuclei in visually-naïve domestic chicks (Gallus gallus).

HighlightsSeptal and amygdaloid nuclei are involved in social behavior of adult animals.Here we investigated their involvement in early social responses of visually naive chicks.Higher activity in septum and amygdaloid nuclei of chicks after the first brief exposure to an alive conspecific. ABSTRACT The septal nuclei are an evolutionarily well‐conserved part of the limbic system, present in all vertebrate groups. Functionally, septal nuclei are involved in many important aspects of social behavior and lateral septum is considered a node of the social decision making network, together with amygdaloid nuclei. Given the importance of septal nuclei for social behaviors, it is somewhat surprising that it has never been investigated whether they are involved in early social responses of naïve animals. In the present study we wanted to know if simple exposure of visually naïve newly hatched chicks to a visual object (an alive, behaving conspecific), that also contains all features to which chicks are known to express early social predispositions, will selectively activate septal areas. We measured brain activity by visualizing the immediate early gene product c‐Fos with a standard immunohistochemical procedure. Notably, after a brief visual exposure to an alive behaving conspecific septum showed higher activation in experimental subjects, compared to baseline animals that were exposed to the same environment in the absence of the conspecific. This is, to the best of our knowledge, the first demonstration of septal involvement in early social responses. We also found similar effects in the nucleus taeniae and arcopallium (amygdala homologues), but not in the medial striatum. This result indicates that at least some nuclei of the social decision making network may participate in early responses to social stimuli. Future studies could capitalize on these results, by identifying the specific visual cues eliciting this effect.

Multiple Visual Field Representations in the Visual Wulst of a Laterally Eyed Bird, the Zebra Finch (Taeniopygia guttata)

The visual wulst is the telencephalic target of the avian thalamofugal visual system. It contains several retinotopically organised representations of the contralateral visual field. We used optical imaging of intrinsic signals, electrophysiological recordings, and retrograde tracing with two fluorescent tracers to evaluate properties of these representations in the zebra finch, a songbird with laterally placed eyes. Our experiments revealed that there is some variability of the neuronal maps between individuals and also concerning the number of detectable maps. It was nonetheless possible to identify three different maps, a posterolateral, a posteromedial, and an anterior one, which were quite constant in their relation to each other. The posterolateral map was in contrast to the two others constantly visible in each successful experiment. The topography of the two other maps was mirrored against that map. Electrophysiological recordings in the anterior and the posterolateral map revealed that all units responded to flashes and to moving bars. Mean directional preferences as well as latencies were different between neurons of the two maps. Tracing experiments confirmed previous reports on the thalamo-wulst connections and showed that the anterior and the posterolateral map receive projections from separate clusters within the thalamic nuclei. Maps are connected to each other by wulst intrinsic projections. Our experiments confirm that the avian visual wulst contains several separate retinotopic maps with both different physiological properties and different thalamo-wulst afferents. This confirms that the functional organization of the visual wulst is very similar to its mammalian equivalent, the visual cortex.

Representation of environmental shape in the hippocampus of domestic chicks (Gallus gallus)

The hippocampus plays an important role in spatial encoding and memory across various vertebrate species. In rodents, hippocampal neurons are particularly sensitive to a change in environmental geometry. Given the similarities in function between the mammalian and avian hippocampi, we aimed to measure whether enclosures varying in geometric shape (square and rectangle) can differentially activate hippocampal cells in the domestic chick (Gallus gallus domesticus). Chicks exposed to both a square and a rectangular arena exhibited a significantly higher neural activation (as measured by c-Fos expression) than those exposed twice to just the square or just the rectangle (both of which were significantly higher in activation than a one-environment control group). For the first time in an avian species, we show that exposure to two enclosures of different geometric shape activates the hippocampus to a greater degree, suggesting a possible effect of spatial remapping.