Martina Manns

Asymmetry pays: visual lateralization improves discrimination success in pigeons

Functional cerebral asymmetries, once thought to be exclusively human, are now accepted to be a widespread principle of brain organization in vertebrates [1]. The prevalence of lateralization makes it likely that it has some major advantage. Until now, however, conclusive evidence has been lacking. To analyze the relation between the extent of cerebral asymmetry and the degree of performance in visual foraging, we studied grain-grit discrimination success in pigeons, a species with a left hemisphere dominance for visual object processing [2,3]. The birds performed the task under left-eye, right-eye or binocular seeing conditions. In most animals, right-eye seeing was superior to left-eye seeing performance, and binocular performance was higher than each monocular level. The absolute difference between left- and right-eye levels was defined as a measure for the degree of visual asymmetry. Animals with higher asymmetries were more successful in discriminating grain from grit under binocular conditions. This shows that an increase in visual asymmetry enhances success in visually guided foraging. Possibly, asymmetries of the pigeons visual system increase the computational speed of object recognition processes by concentrating them into one hemisphere while preventing the other side of the brain from initiating conflicting search sequences of its own.

A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds

The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, “Cluster N”, show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds “see” the reference compass direction provided by the geomagnetic field.

Tectal Mosaic: Organization of the Descending Tectal Projections in Comparison to the Ascending Tectofugal Pathway in the Pigeon

The optic tectum of vertebrates is an essential relay station for visuomotor behavior and is characterized by a set of connections that comprises topographically ordered input from the eyes and an output that reaches premotor hindbrain regions. In the avian tectofugal system, different ascending cell classes have recently been identified based on their dendritic and axonal projection patterns, although comparable information about the descending cells is missing. By means of retrograde tracing, the present study describes the detailed morphology of tectal output neurons that constitute the descending tectobulbar and tectopontine pathways in pigeons. Descending cells were more numerous in the dorsal tectum and differed in terms of 1) their relative amount of ipsi‐ vs. contralateral projections, 2) the location of the efferent cell bodies within different tectal layers, and 3) their differential access to visual input via dendritic ramifications within the outer retinorecipient laminae. Thus, the descending tectal system is constituted by different cell classes presumably processing diverse aspects of the visual environment in a visual field‐dependent manner. We demonstrate, based on a careful morphological analysis and on double‐labeling experiments, that the descending pathways are largely separated from the ascending projections even when they arise from the same layers. These data support the concept that the tectum is arranged as a mosaic of multiple cell types with diverse input functions at the same location of the tectal map. Such an arrangement would enable the tectal projections onto diverse areas to be both retinotopically organized and functionally specific. J. Comp. Neurol. 472:395–410, 2004.

Nucleus isthmi, pars semilunaris as a key component of the tectofugal visual system in pigeons.

The avian isthmic nuclei are constituted by a group of structures reciprocally connected with the tectum opticum and considered to play a role in the modulation of intratectal processes. Although the two larger isthmic nuclei, the n. isthmi pars parvocellularis (Ipc) and the n. isthmi pars magnocellularis (Imc), have been studied in detail previously, the third and smallest of this group, the n. isthmi pars semilunaris (SLu), has been largely neglected. The present study demonstrates this isthmic component to be characterized by a unique connectivity and immunohistochemical pattern: 1) SLu receives tectal afferents and projects back onto the outer retinorecipient tectal layers; 2) it projects bilaterally onto the nucleus rotundus and thus modulates the ascending tectofugal system; 3) in addition, previous studies have demonstrated SLu projections onto the lateral spiriform nucleus (SpL), which mediates basal ganglia output onto the tectum. In that SpL projects onto the deep layers of the tectum, SLu indirectly modulates descending tectal output patterns. Taken together, the role of SLu goes far beyond a local modulation of intratectal processes. Instead, this isthmic structure is likely to play a key role in the topographically organized modulation of the ascending and, at least indirectly, also the descending projections of the optic tectum. J. Comp. Neurol. 436:153–166, 2001.

The eye in the brain: retinoic acid effects morphogenesis of the eye and pathway selection of axons but not the differentiation of the retina in Xenopus laevis

We have analyzed the effects of all-trans retinoic acid (RA) on the morphogenesis, differentiation and projection of the eye of Xenopus. RA was applied in concentrations of 10(-5), 5 x 10(-6) and 10(-6) M at stages 9-17. Animals were reared until stages 40-48. RA applied before stage 11 1/2, abated completely formation of an eye or a retina, at later stages it led to the formation of microphthalmic eyes. Even in the absence of an eye parts of the forebrain had characteristics of the retina, but rods and cones reached then into the lumen of the third ventricle. The projection of eyes of RA-treated animals was revealed with rhodamine dextran amine. Ganglion cell axons projected bilaterally to the tectum, to the hindbrain, the contralateral retina and, occasionally, to the olfactory bulb. RA affects both morphogenesis of the eye and pathway selectivity of ganglion cell axons but not differentiation of the neural retina.

Navigation‐induced ZENK expression in the olfactory system of pigeons (Columba livia)

A large body of evidence indicates that pigeons use olfactory cues to navigate over unfamiliar areas with a differential contribution of the left and right hemispheres. In particular, the right nostril/olfactory bulb (OB) and left piriform cortex (Cpi) have been demonstrated to be crucially involved in navigation. In this study we analysed behaviour‐induced activation of the olfactory system, indicated by the expression of the immediate early gene ZENK, under different homing conditions. One experimental group was released from an unfamiliar site, the second group was transported to the unfamiliar site and back to the loft, and the third group was released in front of the loft. To evaluate the differential contribution of the left and/or right olfactory input, the nostrils of the pigeons were either occluded unilaterally or not. Released pigeons revealed the highest ZENK cell density in the OB and Cpi, indicating that the olfactory system is activated during navigation from an unfamiliar site. The groups with no plug showed the highest ZENK cell density, supporting the activation of the olfactory system probably being due to sensory input. Moreover, both Cpis seem to contribute differently to the navigation process. Only occlusion of the right OB resulted in a decreased ZENK cell expression in the Cpi, whereas occlusion of the left nostril had no effect. This is the first study to reveal neuronal activation patterns in the olfactory system during homing. Our data show that lateralized processing of olfactory cues is indeed involved in navigation over unfamiliar areas.

Monocular deprivation alters the direction of functional and morphological asymmetries in the pigeon's (Columba livia) visual system.

One-day-old pigeons (Columba livia) were monocularly deprived by occluding the left or the right eye for 10 days. Up to 3 years later, degree and direction of functional and morphological asymmetries of deprived and control pigeons were analyzed. In control pigeons, the usual right-eye superiority was obtained in a visual discrimination task. In left-eye deprived pigeons, this behavioral asymmetry was strengthened, whereas the direction of lateralization was reversed in right-eye deprived birds. A morphological tectum analysis revealed that control and left-eye deprived pigeons displayed similar asymmetries, with the left-monocular deprived pigeons exhibiting more pronounced left-right differences. Tectal morphometry of right-eye deprived pigeons displayed a reversed pattern. Overall, the present study shows that a short period of posthatch monocular deprivation is sufficient to alter behavioral and morphological visual asymmetry for several years.

Light experience induces differential asymmetry pattern of GABA- and parvalbumin-positive cells in the pigeon's visual midbrain

The formation of functional and morphological asymmetries within the pigeons tectofugal system depends on left-right differences in visual input during embryonic development. This asymmetric stimulation presumably affects activity-dependent differentiation processes within the optic tectum. Behavioral studies reveal that prehatch light stimulation asymmetry influences both left- and right-hemispheric processes in a differential way. Thus, we have to assume divergent effects on both hemispheres. This study represents an attempt to test the hypothesis that embryonic light asymmetry induces different, cell-type-specific effects in the left and the right optic midbrain. Since it is likely that inhibitory interneurons play a critical role in the establishment of asymmetries, we examined in both sides of the brain the soma sizes of GABA- and parvalbumin- (PV) immunoreactive (ir) cells of the tectum and the magnocellular isthmic nucleus in controls and in dark-incubated animals. No cell size asymmetries of magnocellular isthmic neurons were found in either dark-incubated or control birds. Dark-incubation also prevented the establishment of lateralized differences in GABAergic and PV-positive tectal cells. However, in control birds GABAergic cells displayed larger somata in the left tectum, whereas PV-ir neurons were enlarged within the right tectum. This complementary asymmetry pattern suggests that PV- and GABA-ir tectal cells represent different cellular populations which react differently to visual input. Thus, our data show that visual lateralization does not result from a mere growth promoting effect that enhances differentiation within the behaviorally dominant left side, but is constituted by different cell type-specific circuits which are divergently adjusted in the left and in the right tectum.

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.

Dual coding of visual asymmetries in the pigeon brain: the interaction of bottom-up and top-down systems

The pigeon’s visual system is an excellent model to investigate the ontogenetic and the neuronal foundations of cerebral asymmetries. Before hatching, lateralized visual stimulation induces structural asymmetries within the tectofugal pathway during a critical time window. Interhemispheric control mechanisms emerge presumably after hatching and stabilize these induced asymmetries. Once established, visual asymmetry in pigeons displays a left hemispheric dominance for complex learning and discrimination tasks and unravels how the interplay between bottom-up and top-down mechanisms generate a lateralized, hemispheric-specific visual analysis. The ascending visual (tectofugal) pathway displays cell size asymmetries and directs more bilateral visual information towards the left hemisphere. This bottom-up system is controlled by telencephalic top-down projections, which affect intra- and/or interhemispheric inhibitory systems in a presumably lateralized manner. Such a flexible organization allows the control of information transfer depending on the visual input and hence adapt the dominant processing mode to environmental requirements.