Embryonic Light Stimulation 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‐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.

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.

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.

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.

Embryonic light stimulation induces different asymmetries in visuoperceptual and visuomotor pathways of pigeons

In birds, visual object discrimination performance is lateralized with a dominance of the right eye/left hemisphere. This asymmetry is induced by embryonic light stimulation. However, visually guided behavior, even during simple object distinction tasks, is composed of different behavioral and neural modules. Therefore, the aim of the present study was to test whether all neural subsystems involved in visual discriminations are lateralized in a similar way after prehatch visual stimulation. To examine this question, two behavioral paradigms were used which reveal complementary aspects of visually guided behavior. The first was the grain–grit discrimination task in which no left–right differences in the number of pecks, but significant differences in the number of grains can be found. Therefore, grain–grit discrimination reveals visuoperceptual performance but not visuomotor speed. The contrary seems to be the case for a successive pattern discrimination with a VR32 schedule. Here, the hemispheres do not differ with respect to discrimination accuracy but with regard to the number of pecks emitted. Thus, successive pattern discrimination with lean VR schedules reveals hemispheric differences in visuomotor speed without testing visuoperceptual performance. Using these two paradigms a group of light and a group of dark incubated pigeons were tested. The results show that dark incubated birds evinced no asymmetry in any measure while light incubated ones were right-eye dominant in both variables. However, light incubation induced a visual left hemispheric dominance by modulating two different processes, a left-hemispheric increase of visuoperceptual processes; and a right-hemispheric decrease for visuomotor speed. Taken together these data show that embryonic light stimulation elicits visual lateralization by differently modulating visuoperceptual and visuomotor systems in both hemispheres.