Asymmetries in visuospatial processing in birds

Contents

Abstract

Introduction

Methods

Results

Discussion

References

Abstract

Cerebral asymmetries are a fundamental principle of vertebrate brain architecture. These asymmetrical structures are most likely beneficial for various kinds of information processings. Research has shown that the avian brain is highly visually-lateralized. Results display a left hemisphere/right eye advantage in pigeons for object processing. Unfortunately, findings on visuospatial lateralization are ambiguous. In chicks also a left hemisphere dominance for object processing has been shown whereas the right hemisphere is more probable to elicit high performances in visuospatial tasks. Inconsistently, homing pigeons revealed a left-hemispheric superiority for visuospatial orientation. We investigated visuospatial processing in pigeons (Columba livia) with a new experimental paradigm. The subjects were confined in a box with their neck and head protruding through a central circular opening. This opening was surrounded by sixteen concentrically arranged food positions each containing one piece of grain the animals had to peck at. Pigeons were tested alternately under monocular (left/right) and binocular conditions. We measured the time the subjects needed to peck all grains and the extent of visual scanning, operationalized by crossing the circular segments with their head. Although both monocular conditions did not differ with respect to the time needed to finish the task, right-seeing animals needed fewer scans to finish the task. Remarkably, both monocular conditions did not reveal significant differences in number of divers, number of peckfailures and number of direction changes. These findings display a higher efficiency of left hemispheric visuospatial processing. Left-seeing pigeons needed more scans per time than right-seeing birds to consume the grains. In summary, the superiority of the right hemisphere in spatial tasks is not an universal phenomenon of vertebrate brain architecture.

Keywords: Lateralization, spatial represenation, visuospatial processing

Introduction

The present study investigates the effects of cerebral asymmetries on visuospatial processing in the avian brain. The avian brain seems to be highly suitable for research on lateralization patterns in vertebrates. Eventually, the question might arise why the effects of asymmetry in vertebrates are focus of investigation in psychological research. Many neuronal disorders (schizophrenia, autism, etc.) are proved to result from lateralization patterns deviating from the normal structure (Highley et al. 2002). Due to the fact that nearly all cognitive functions are lateralized lateralization is one of the most fundamental principles of the brain providing optimal processing and integration of information (Rogers 2000). Unfortunately, this phenomenon has been claimed to be exclusively human for several years. Today, it is known that lateralization is widespread among vertebrates and we also know that specifcally the avian brain is predestined to research on due to particular ontogenetic factors. A lot of research has been conducted e.g. on the pigeons’ visual system and the cerebral lateralization of information processing, but investigations primarely focus on visual discrimination tasks (e.g. Skiba et al. 2001) and working-memory tasks (e.g. Prior and Güntürkün 2001). This study intends to provide more information on the spatial representation of visual stimuli in pigeons. Unfortunately, asymmetry research has neglected the question in what way the pigeon brain is lateralized with regard to visuospatial processing. Especially when investigating the effects of lateralization on spatial representation mainly experiments on homing pigeons have been conducted (Ulrich et al. 1999). In the subsequent paragraphs the characteristic features of the avian brain lateralization are revealed in detail.

The avian visual system

An important advantage of researching the avian cerebral lateralization results from the visual pathways’ organisation: visual information is processed by two visual pathways (Rogers 1996) – the tectofugal and thalamofugal visual system. The tectofugal system projects from the retina to the contrallateral optic tectum. From the optic tecta it projects to the ipsilateral and contrallateral nucleus rotondus. Finally, information being processed arives the ipsilateral region of the forebrain (Benowitz and Karten 1976; Karten and Hodos 1970). In the thalamofugal system visual information reaches the forebrain hemispheres by projections from the retina to the contralateral nucleus opticus principialis thalami (OPT) in the dorsolateral thalamus (Karten et al. 1973). The OPT projects mainly to the ipsilateral hyperstriatial forebrain, few projections also reach the contralateral hyperstratium. The avian brain is predestined to research lateralization effects: by occluding one eye dominating performance of the contralateral hemisphere can be assumed. These two visual pathways which have been found in the avian brain process different kind of visual stimuli. Research on pigeons has shown that processing of coloured stimuli, detection of movement and pattern discrimination involves (Hodos 1969; Hodos and Karten 1970) the tectofugal pathway. The role of the thalamofugal system is controversial: some findings support the thesis that the thalamofugal system is involved in acquisition and revearsal of spatial discrimination (Macphail and Reilly 1989), other findings could prove that the OPT is more likely to detect stimuli in the lateral field leading to head movements finally resulting in focussing the stimuli in the frontal, binocular visual field (Güntürkün et al. 1989). In pigeons the tectofugal pathway dominates the processing of visual stimuli; approximately 90% of retinal ganglion cells belong to the tectofugal system (Hellman and Güntürkün 2001). Furthermore, structural differences between the left and right tectofugal system have been reported (Güntürkün 1997; Güntürkün and Hahmann 1999; Manns and Güntürkün 1999a; Manns and Güntürkün 1999b). A greater extent of bilateral representations in the left tectofugal system (Güntürkün et al. 1998) and an asymmetrical arrangement of transcommissural interactions over midbrain commissures have been found (Keysers et al. 2000). Güntürkün (1993) also found that somata cells of the right-sided lamina and the retinorecipient layers of the left tectum are larger than in the right tectum. These neuroanatomical asymmetries lead to particular behavioural left-right differences (Skiba et al. 2002). The left-right differences emerge as a product of several ontogentic factors: pigeon and also chick visual lateralization has been proved to be triggered by short light exposure before hatch (Rogers 1996). The birds’ posture in the eggs leads to asymmetrical light stimulation of the eyes and therefore, different activation levels in the left and right hemisphere are likely to occur which is due to the the specific organisation of the visual pathways (s.a. for detailed explanation). In the egg the birds’ head is turned to the right so that the left eye is very close to the body hardly receiving any light stimulation whereas the right eye directly lies beneath the translucant shell (Kuo 1932). This asymmetrical light stimulation effects the modulation of synaptic patterns of the ascending pathways resulting in a left-hemispheric dominance with regard to visual processing. Through the translucant shell light stimulates the retina cells in the right eye of the birds, synaptic patterns connecting the right eye with the left hemisphere are modulated leading to higher performance levels of the left hemisphere (Güntürkün 1993). The development of hemispherical superiority can be hindered by dark incubation of birds’ eggs. I.e. lacking of any light stimulation during breeding prevents the occurence of synaptic modulation as found under natural conditions. Comparing light and dark incubated birds several significant differences in visual tasks can be found. Skiba et al. (2001) found that embryonic light stimulation in pigeons induces particular asymmetries in visual pathways. By using two experimental paradigms – the “grain-grit discrimination task” and “successive discrimination with a VR 32 schedule” they showed that embryonic light stimulation in pigeons differently modulates visuopercetual and visuomotor systems. Güntürkün and Kesch (1987) also demonstrated in a previous study that pigeons revealed a left hemisphere dominance for visually guided behaviour in the grain-grit task in which the subjects have thirty seconds time to detect and to consume thirty grains out of thousand pebbles having the same color, shape and size as the real grains. Under monocular viewing conditions light incubated pigeons displayed significant better performances in both visuoperceptual and visuomotoric task when using their right eye. In addition, Skiba et al. (2001) found that dark incubated pigeons did not reveal a significant difference between both monocular seeing conditions during both tasks. Concluding, light incubation induces left hemispheric dominance by increasing the capacity of the left hemisphere during visuoperceptual processes and decreasing the right hemisphere’s capacity during visuomotoric processes. Preceeding research on lateralization in pigeons indicates a major advantage of left-hemisphere/right eye performance in visual tasks. Diekamp et al. (1999) investigated lateralization of color reversal learning in pigeons. They found that pigeons revealed faster improvement and lower error rates when performing with their right eye after acquiring a simple color discrimination.

In summary, pigeon visual lateralization leads to more efficient performances in tasks involving visual discrimination. The question predominating the present study is in what way visual lateralization also effects performance levels in visuospatial tasks. Some evidence supports the thesis that in the avian brain, especially in chicks, the right-hemisphere mainly contributes to spatial cognition involving the construction of topographical maps (Rashid and Andrew 1989) whereas the left hemisphere elicits better visual discrimation performance (Bradshaw and Rogers 1993). These findings are consistent with results found in human experiments (Hellige and Michimata 1989; Hellige 1995). In chicks Regolin and Vallortigara (1995) showed that global spatial information is mainly processed by the right hemisphere wheras object-specific cues are mainly managed by the left hemisphere. Research on visuospatial lateralization in bottlenose dolphins (Tursiops truncatus) is inconsistent with findings in chicks and humans. Kilian et al. (2000) tested two bottlenose dolphin in a visuospatial task. In this task the subjects were placed in a circular tank in which they had to swim from a starting position through three hoops vertically arranged in a row. A correct trial required passing each hoop only once and returning to the starting position after swimming through each hoop. This task measured the quality of the spatial representation of the arena the dolphins were tested in. The subjects were tested under monocular (left/right) and binocular conditions. Right-seeing dolphins displayed significant better performance, operationalized by the number of correct trials. These findings point to a more elaborate spatial representation under left hemisphere/right-eye performance indicating that the superiority of the right hemisphere in spatial tasks is not an universal principle of vertebrate brain architecture. Evidence for this thesis was found by Ulrich et al. (1999) by showing left-hemispheric superiority for visuospatial orientation in homing pigeons. They tested lateralization of visuospatial orientation by releasing pigeons from different release sites and measuring their homing performance under two monocular (left/right) and binocular conditions. Birds using their right eye showed significantly better homing performance measured by homing times. Additionally, these results provide further proof of the existence of deviations from previous findings in which the right hemisphere dominantes in spatial cognition. However, the conclusion Ulrich et al. (1999) have drawn is disputable since the pigeons might have used a particular strategy of visual memory snapshot tracking to pursue visual features along the learned route. Thus, a left-hemispheric dominance could be explained by better memory and visual discrimination performance which pigeons are known to show under right-seeing conditions (Braithwhaite and Guilford 1995). Furthermore, it was hypothized that the effect of left hemispheric dominance might vanish if pigeons were tested in a maze excluding the use of the visual memory strategy (Hellige 1993). In the present study we intended to show a left hemispheric superiority for spatial representation in pigeons tested in a new experimental paradigma which excludes the use of certain strategies as the subjects might have had of their disposal during homing experiments probably leading to apparant left hemisphere dominances. We assume that the right hemisphere’s prevalence is not an universal principle which can be found consistently among all vertebrates and hypothized that contrary to finding in chicks (Tommasi and Vallortigara 2001) and other species there is a more efficient performance of the left hemisphere/right eye in pigeons when conducting a spatial representation task. For this reason, we expect to replicate the findings Ulrich et al. (1999) made and to find indisputable proof of a left hemispheric prevalence during spatial information processing.

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