Embryonic Light Research Articles

Unlocking the symmetric transfer of irrelevant information: gene-environment interplay and enhanced interhemispheric cross-talk.

Hemispheric specialization influences stimulus processing and behavioural control, affecting responses to relevant stimuli. However, most sensory input is irrelevant and must be filtered out to prevent interference with task-relevant behaviour, a process known as habituation. Despite habituation's vital role, little is known about hemispheric specialization for this brain function. We conducted an experiment with domestic chicks, an elite animal model to study lateralization. They were exposed to distracting visual stimuli while feeding when using binocular or monocular vision. Switching the viewing eye after habituation, we examined if habituation was confined to the stimulated hemisphere or shared across hemispheres. We found that both hemispheres learned equally to ignore distracting stimuli. However, embryonic light stimulation, influencing hemispheric specialization, revealed an asymmetry in interhemispheric transfer of the irrelevant information discarded via habituation. Unstimulated chicks exhibited a directional bias, with the right hemisphere failing to transfer distracting stimulus information to the left hemisphere, while transfer from left to right was possible. Nevertheless, embryonic light stimulation counteracted this asymmetry, enhancing communication from the right to the left hemisphere and reducing the pre-existing imbalance. This sharing extends beyond hemisphere-specific functions and encompasses a broader representation of irrelevant events.

Light-incubation effects on lateralisation of single unit responses in the visual Wulst of domestic chicks

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.

Effect of embryonic light exposure on laterality and sociality in quail chicks (Coturnix coturnix japonica)

Lateralization is the ascendency of one side of the body or the brain to control and perform motor or perceptual functions. Light exposure during prenatal life can modulate the expression of visual lateralization (strength and direction) in a variety of species, including birds. Individual lateralization provides cognitive advantages, but the function of lateralization at the population level is less obvious. Recent studies support the hypothesis that intra-specific population-level lateralization may favour coordination between asymmetrical individuals during synergistic (cooperative) social interactions. Since cohesion requires a good coordination, one can therefore imagine that a higher alignment of lateralization within a group, by making coordination between individuals easier, may promote social cohesion. Our study investigated the effect of light on laterality and social behaviour in Japanese quail chicks (Coturnix coturnix japonica). We compared chicks coming from eggs exposed to light during incubation to chicks coming from eggs maintained in complete darkness. We expected light-exposed (LE) chicks to be more aligned than dark-incubated (DI) ones and we wanted to test whether the most aligned chicks were also the most coordinated. We assessed laterality, social motivation, synchronization and spatial cohesion within groups of LE and DI chicks. The prenatal light conditions did not affect either laterality or chicks’ social behaviour, and there was no turning bias at the group level. An absolute laterality index characterizing the alignment of chicks living together showed that the groups with the highest indices were not necessarily the groups with the greatest synchronization and spatial cohesion. This suggests that light does not consistently induce laterality in Japanese quail chicks and that the alignment of the chicks’ turning bias does not influence their social cohesion. Quails are widely used in farm industry and scientific research and better knowledge of the consequences of incubation conditions on their behavioural asymmetries and sociality could help improve their handling and welfare.

Light‐dependent development of the tectorotundal projection in pigeons

Left-right differences in the structural and functional organization of the brain are widespread in the animal kingdom and develop in close gene-environment interactions. The visual system of birds like chicks and pigeons exemplifies how sensory experience shapes lateralized visual processing. Owing to an asymmetrical posture of the embryo in the egg, the right eye/ left brain side is more strongly light-stimulated what triggers asymmetrical differentiation processes leading to a left-hemispheric dominance for visuomotor control. In pigeons (Columba livia), a critical neuroanatomical element is the asymmetrically organized tectofugal pathway. Here, more fibres cross from the right tectum to the left rotundus than vice versa. In the current study, we tested whether the emergence of this projection asymmetry depends on embryonic light stimulation by tracing tectorotundal neurons in pigeons with and without lateralized embryonic light experience. The quantitative tracing pattern confirmed higher bilateral innervation of the left rotundus in light-exposed and thus, asymmetrically light-stimulated pigeons. This was the same in light-deprived pigeons. Here, however, also the right rotundus received an equally strong bilateral input. This suggests that embryonic light stimulation does not increase bilateral tectal innervation of the stronger stimulated left but rather decreases such an input pattern to the right brain side. Combined with a morphometric analysis, our data indicate that embryonic photic stimulation specifically affects differentiation of the contralateral cell population. Differential modification of ipsi- and contralateral tectorotundal connections could have important impact on the regulation of intra- and interhemispheric information transfer and ultimately on hemispheric dominance pattern during visual processing.

Distinct effect of early and late embryonic light-stimulation on chicks' lateralization

Embryonic light exposure affects similarly functional lateralization in fish and birds. While the light acts on an asymmetric habenular system during the first post fertilization hours in zebrafish, in the domestic chicks it shapes the thalamofugal visual pathway affecting the right retinal photoreceptors in the last stages before hatching. However, recent evidence has shown that also in chicks a precocial embryonic time window seems open to light action. Here we addressed the issue of whether the light effect is comparable in the early and late sensitive periods of chicks' embryonic development by testing birds coming from early (EL) and late (LL) light stimulated eggs compared to dark maintained eggs (DK) under different conditions of vision in a gravel-grain task. The perseveration of pecks directed to irrelevant elements revealed that in all chicks the right hemisphere was heavily attracted by the novel elements when tested with the left eye. When using the right eye, instead, only DK chicks attended repeatedly to distractors whereas LL and EL chicks showed a left hemisphere advantage for fine discrimination and sustained attention; conversely, when tested binocularly, LL chicks perseverated significantly more than both DK and EL chicks, likely compensating the distraction with the analysis carried out by both hemispheres. For the first time, we unveiled a fine graded difference between the light modulation exerted during the two time windows, adding evidence to the idea that genes and environmental factors interplay in several separate routes to the modulation of the neurodevelopment of cerebral lateralization in vertebrates.

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.

Development of the Astyanax mexicanus circadian clock and non-visual light responses

Most animals and plants live on the planet exposed to periods of rhythmic light and dark. As such, they have evolved endogenous circadian clocks to regulate their physiology rhythmically, and non-visual light detection mechanisms to set the clock to the environmental light-dark cycle. In the case of fish, circadian pacemakers are not only present in the majority of tissues and cells, but these tissues are themselves directly light-sensitive, expressing a wide range of opsin photopigments. This broad non-visual light sensitivity exists to set the clock, but also impacts a wide range of fundamental cell biological processes, such as DNA repair regulation. In this context, Astyanax mexicanus is a very intriguing model system with which to explore non-visual light detection and circadian clock function. Previous work has shown that surface fish possess the same directly light entrainable circadian clocks, described above. The same is true for cave strains of Astyanax in the laboratory, though no daily rhythms have been observed under natural dark conditions in Mexico. There are, however, clear alterations in the cave strain light response and changes to the circadian clock, with a difference in phase of peak gene expression and a reduction in amplitude. In this study, we expand these early observations by exploring the development of non-visual light sensitivity and clock function between surface and cave populations. When does the circadian pacemaker begin to oscillate during development, and are there differences between the various strains? Is the difference in acute light sensitivity, seen in adults, apparent from the earliest stages of development? Our results show that both cave and surface populations must experience daily light exposure to establish a larval gene expression rhythm. These oscillations begin early, around the third day of development in all strains, but gene expression rhythms show a significantly higher amplitude in surface fish larvae. In addition, the light induction of clock genes is developmentally delayed in cave populations. Zebrafish embryonic light sensitivity has been shown to be critical not only for clock entrainment, but also for transcriptional activation of DNA repair processes. Similar downstream transcriptional responses to light also occur in Astyanax. Interestingly, the establishment of the adult timing profile of clock gene expression takes several days to become apparent. This fact may provide mechanistic insight into the key differences between the cave and surface fish clock mechanisms.

Visuospatial attention in the lateralised brain of pigeons \u2013 a matter of ontogenetic light experiences

The ontogenetic mechanisms leading to complementary hemispheric specialisations of the two brain halves are poorly understood. In pigeons, asymmetrical light stimulation during development triggers the left-hemispheric dominance for visuomotor control but light effects on right-hemispheric specialisations are largely unknown. We therefore tested adult pigeons with and without embryonic light experience in a visual search task in which the birds pecked peas regularly scattered on an area in front of them. Comparing the pecking pattern of both groups indicates that the embryonic light conditions differentially influence biased visuospatial attention under mono- and binocular seeing conditions. When one eye was occluded, dark-incubated pigeons peck only within the limits of the visual hemifield of the seeing eye. Light-exposed pigeons also peck into the contralateral field indicating enlarged monocular visual fields of both hemispheres. While dark-incubated birds evinced an attentional bias to the right halfspace when seeing with both eyes, embryonic light exposure shifted this to the left. Thus, embryonic light experience modifies processes regulating biased visuospatial attention of the adult birds depending on the seeing conditions during testing. These data support the impact of light onto the emergence of functional dominances in both hemispheres and point to the critical role of interhemispheric processes.

Early- and Late-Light Embryonic Stimulation Modulates Similarly Chicks’ Ability to Filter out Distractors

Chicks (Gallus gallus) learned to run from a starting box to a target located at the end of a runway. At test, colourful and bright distractors were placed just outside the starting box. Dark incubated chicks (maintained in darkness from fertilization to hatching) stopped significantly more often, assessing more the left-side distractor than chicks hatched after late (for 42 h during the last three days before hatching) or early (for 42 h after fertilization) exposure to light. The results show that early embryonic light stimulation can modulate this particular behavioural lateralization comparably to the late application of it, though via a different route.

The effects of light exposure during incubation on embryonic development and hatchling traits in lizards.

Light is an environmental factor that is known to profoundly affect embryonic development in some oviparous vertebrates, but such effects are unstudied in reptiles. We investigated the light sensitivity of lizard embryos by examining the thickness and light transmittance of eggshells as well as the effect of light on embryonic development and hatchling traits in four lizard species, the Chinese skink (Plestiodon chinensis), the northern grass lizard (Takydromus septentrionalis), the oriental leaf-toed gecko (Hemidactylus bowringii) and the Japanese gecko (Gekko japonicus). The eggshells were thinner and thus had higher light transmittance in Chinese skink than the other three species. Light exposure during incubation significantly accelerated the embryonic development in all species, with higher light intensity resulting in faster embryonic development. Interestingly, light stimulation negatively influenced hatchling size and survival in skinks, but had no effect in lacertids and geckos. This interspecific discrepancy not only relates to the differences in thickness and light transmittance of eggshells, but might also reflect the differences in the reproductive habits of these species. Given the diversity of light conditions that reptile embryos face during development, studies on the response of reptile embryos to light may offer a unique opportunity to understand the mechanisms of embryonic light sensitivity in animals.

Cryptochrome 1b: a possible inducer of visual lateralization in pigeons?

The visual system of adult pigeons shows a lateralization of object discrimination with a left hemispheric dominance on the behavioural, physiological and anatomical levels. The crucial trigger for the establishment of this asymmetry is the position of the embryo inside the egg, which exposes the right eye to light falling through the egg shell. As a result, the right-sided retina is more strongly stimulated with light during embryonic development. However, it is unknown how this embryonic light stimulation is transduced to the brain as rods and cones are not yet functional. A possible solution could be the blue-light-sensitive molecule cryptochrome 1 (Cry1), which is expressed in retinal ganglion cells (RGCs) of several mammalian and avian species. RGCs have been shown to be functional during the time of induction of asymmetry and possess projections to primary visual areas. Therefore, Cry1-containing RGCs could be responsible for induction of asymmetry. The aim of this study was to identify the expression pattern of the Cry1 subtype Cry1b in the retina of embryonic, post-hatch and adult pigeons by immunohistochemical staining and to show whether Cry1b-containing RGCs project to the optic tectum. Cry1b-positive cells were indeed mainly found in the RGC layer and to lesser extent in the inner nuclear layer at all ages, including the embryonic stage. Tracing in adult animals revealed that at least a subset of Cry1b-containing RGCs project to the optic tectum. Thus, Cry1b-containing RGCs within the embryonic retina could be involved in the induction of asymmetries in the visual system of pigeons.

Shaping a lateralized brain: Asymmetrical light experience modulates access to visual interhemispheric information in pigeons

Cerebral asymmetries result from hemispheric specialization and interhemispheric communication pattern that develop in close gene-environment interactions. To gain a deeper understanding of developmental and functional interrelations, we investigated interhemispheric information exchange in pigeons, which possess a lateralized visual system that develops in response to asymmetrical ontogenetic light stimulation. We monocularly trained pigeons with or without embryonic light experience in color discriminations whereby they learned another pair of colors with each eye. Thereby, information from the ipsilateral eye had to be transferred. Monocular tests confronting the animals with trained and transferred color pairs demonstrated that embryonic light stimulation modulates the balance of asymmetrical handling of transfer information. Stronger embryonic stimulation of the left hemisphere significantly enhanced access to interhemispheric visual information, thereby reversing the right-hemispheric advantage that develops in the absence of embryonic light experience. These data support the critical role of environmental factors in molding a functionally lateralized brain.

Early-light embryonic stimulation suggests a second route, via gene activation, to cerebral lateralization in vertebrates

Genetic factors determine the asymmetrical position of vertebrate embryos allowing asymmetric environmental stimulation to shape cerebral lateralization. In birds, late-light stimulation, just before hatching, on the right optic nerve triggers anatomical and functional cerebral asymmetries. However, some brain asymmetries develop in absence of embryonic light stimulation. Furthermore, early-light action affects lateralization in the transparent zebrafish embryos before their visual system is functional. Here we investigated whether another pathway intervenes in establishing brain specialization. We exposed chicks' embryos to light before their visual system was formed. We observed that such early stimulation modulates cerebral lateralization in a comparable vein of late-light stimulation on active retinal cells. Our results show that, in a higher vertebrate brain, a second route, likely affecting the genetic expression of photosensitive regions, acts before the development of a functional visual system. More than one sensitive period seems thus available to light stimulation to trigger brain lateralization.

The impact of asymmetrical light input on cerebral hemispheric specialization and interhemispheric cooperation

Hemispheric specialization potentially provides evolutionary advantages by enhancing cognitive capacities. However, separation of function might be advantageous only with the presence of commissural systems allowing for efficient information exchange and cooperation between the hemispheres. Here we investigate hemispheric cooperation in pigeons as they possess an asymmetrically organized visual system that develops in response to biased ontogenetic light stimulation. This allows comparison of the integration capacities of lateralized (light-incubated) and non-lateralized (dark-incubated) animals. We show that pigeons integrate information learnt separately with each hemisphere when confronted with a transitive reasoning task that they cannot solve with the knowledge of one hemisphere alone. Impairments in dark-incubated birds demonstrate that this ability depends on asymmetrical embryonic light stimulation. Our study provides for the first time direct evidence that lateralized environmental experience not only induces hemispheric specialization, but also affects the efficiency of interhemispheric crosstalk. Environmental factors can influence the tight interplay between the hemispheres, which in turn determines cognitive abilities.

Pseudoneglect and embryonic light stimulation in the avian brain.

A bias to allocate attention to the left hemispace, similar to the well-known pseudoneglect phenomenon shown by humans, has been recently reported in domestic chicks and other species of birds. Asymmetrical light exposure of the embryo of the domestic chick in a critical period before hatching is known to be responsible for a structural asymmetry in the visual ascending projections of the thalamofugal pathway and for lateralization of some visual behaviors. Thus the animal model provided by the chick makes possible investigation of the prenatal factors that may influence asymmetry in spatial attention. Here chicks coming from eggs exposed to light (light incubated, Li-chicks) and chicks incubated in darkness (dark incubated, Di-chicks) were tested in a task in which they were required to explore an area in front of them and to sample grains of food. The results showed that Li-chicks attended more to target stimuli located in the left hemispace, whereas no asymmetry was shown by Di-chicks. When grains of food were presented with small novel pebbles as distractors, both Li- and Di-chicks tended to allocate attention toward the left hemispace. When, however, chicks were tested after familiarization with pebbles, no bias was shown by either Li- and Di-chicks. Hence it seems that cerebral lateralization associated with right hemispheric involvement in response to novelty, interacts with the modulatory effect of asymmetric embryonic light stimulation on preferential allocation of spatial attention in the left hemispace (right hemisphere) and right eye (left hemisphere) control of visual discrimination during feeding.

Patterns of early embryonic light exposure determine behavioural asymmetries in zebrafish: A habenular hypothesis

Releasers of innate responses are more effective in many vertebrates when seen by the left eye. In zebrafish Brachydanio rerio, this asymmetry is linked with neuroanatomical asymmetry of the habenular complex (enlarged left lateral and right medial habenular nuclei): if habenular asymmetry is reversed, reader response to releasers shifts to the right eye. Light exposure (schedule: 14/10 h, L/D) during the first few days of development post fertilisation (pf) controls the patterning of this asymmetry. We show here, using response to a model predator on day 7 pf, that absence of light on day 1 pf alone causes high responsiveness to shift from left to right eye and to intensify. Absence on day 2 pf or day 3 pf produces lesser shifts, whereas absence for all 3 days reduces responsiveness without any shift. Action on day 1 pf is likely to be due to modulation of gene expression. A known disturbance of gene ( nrp1a) expression causes rerouting of the outflow of the left lateral habenula to the way station of the right medial habenula, providing a possible explanation of shifts. Variation in exposure of eggs to light is likely to produce inter-individual variation in the field.

Effects of embryonic light stimulation on the ability to discriminate left from right in the domestic chick

Following an early suggestion by Mach [Mach E. The analysis of sensations. Chicago: Open Court Publishing House; 1897 [reprinted by Dover Publications, 1959]] it has been claimed that brain asymmetry would be crucial for biological organisms in order to discriminate left from right. However, direct evidence in support of this hypothesis is scanty. In the animal system model provided by the newly hatched domestic chick ( Gallus gallus) it has been proved feasible to manipulate lateralization on visual tasks by exposing the eggs to light for a brief period before hatching. The light exposure leads to the development of lateralization of some visual functions and generates asymmetry in the thalamofugal visual projections to the forebrain, because the late-stage embryo is turned in the egg so that it occludes its left but not its right eye. Thus, it is possible to obtain organisms with strong (light-incubated chicks, Li-chicks) or weak (dark-incubated chicks, Di-chicks) lateralization. Li- and Di-chicks were trained to discriminate between two small beads for food reward on the basis of their relative left–right position. Li-chicks performed better than Di-chicks. In order to check whether Di-chicks showed a general impairment in discrimination learning, not confined to left–right discrimination only, chicks were tested in a spatial re-orientation task in a square-shaped arena, in which a target located in a corner could be identified using the left–right location of a conspicuous cue (the colour of a wall) which could be used as a landmark. Results showed that Di-chicks were impaired with respect to Li-chicks in use of left–right information for re-orientation, but not in use of the cue as a landmark. These results provide direct evidence that modulation of the strength of visual lateralization may affect left–right discrimination abilities.

Breaking the balance: Ocular BDNF‐injections induce visual asymmetry in pigeons

In pigeons, asymmetric photic stimulation around hatch induces functional visual asymmetries that are accompanied by left-right differences in tectal cell sizes. Different aspects of light-dependent neuronal differentiation are known to be mediated by the brain-derived neurotrophic factor (BDNF). Therefore, we investigated by means of single or triple BDNF- or saline-injections into the right eye of dark-incubated pigeon hatchlings if ocular BDNF enrichment mimics the effects of biased visual input. As adults, the birds were tested in a grit-grain discrimination task to estimate the degree and direction of visual lateralization followed by a morphometric analysis of retinal and tectal cells. The grit-grain discrimination task demonstrated that triple BDNF-injections enhanced visuoperceptual and visuomotor functioning of the left eye system. Morphometric analysis showed bilateral cell-type dependent effects within the optic tectum. While single-BDNF injections increased cell body sizes of calbindin-positive efferent neurons, triple-injections decreased cell sizes of parvalbumin-positive cells. Moreover, single BDNF-injections increased retinal cell sizes within the contralateral eye. Analysis of BDNF-induced intracellular signaling demonstrated enhanced downstream Ras activation for at least 24 h within both tectal halves whereas activity changes within the contralateral retina could not be detected. This points to primarily tectal effects of ocular BDNF. In sum, exogenous BDNF modulates the differentiation of retinotectal circuitries and dose-dependently shifts lateralized visuomotor processing towards the noninjected side. Since these effects are opposite to embryonic light stimulation, it is unlikely that the impact of light onto asymmetry formation is mediated by retinal BDNF.

Early embryonic light detection improves survival

Early embryonic light detection improves survival

Early embryonic light detection improves survival

Classically, organization of the vertebrate circadian clock was seen as highly centralized in specific neural structures. Over recent years, this view has been transformed dramatically toward a more decentralized model with a number of distinct peripheral tissue clocks [1,2]. This is particularly true of zebrafish, where adult tissues contain autonomous circadian oscillators, which respond directly to light [3,4]. Cell lines derived from 24 hour old zebrafish embryos show the same circadian and light responsiveness as adult tissue [4,5].