Burkhard Hellmann

Structural Organization of Parallel Information Processing Within the Tectofugal Visual System of the Pigeon

Visual information processing within the ascending tectofugal pathway to the forebrain undergoes essential rearrangements between the mesencephalic tectum opticum and the diencephalic nucleus rotundus of birds. The outer tectal layers constitute a two‐dimensional map of the visual surrounding, whereas nucleus rotundus is characterized by functional domains in which different visual features such as movement, color, or luminance are processed in parallel. Morphologic correlates of this reorganization were investigated by means of focal injections of the neuronal tracer choleratoxin subunit B into different regions of the nuclei rotundus and triangularis of the pigeon. Dependent on the thalamic injection site, variations in the retrograde labeling pattern of ascending tectal efferents were observed. All rotundal projecting neurons were located within the deep tectal layer 13. Five different cell populations were distinguished that could be differentiated according to their dendritic ramifications within different retinorecipient laminae and their axons projecting to different subcomponents of the nucleus rotundus. Because retinorecipient tectal layers differ in their input from distinct classes of retinal ganglion cells, each tectorotundal cell type probably processes different aspects of the visual surrounding. Therefore, the differential input/output connections of the five tectorotundal cell groups might constitute the structural basis for spatially segregated parallel information processing of different stimulus aspects within the tectofugal visual system. Because two of five rotundal projecting cell groups additionally exhibited quantitative shifts along the dorsoventral extension of the tectum, data also indicate visual field–dependent alterations in information processing for particular visual features. J. Comp. Neurol. 429:94–112, 2001.

Asymmetries of representation in the visual system of pigeons

ALTHOUGH functional asymmetries in the course of visual information processing have been known for a long time in humans as well as in non-human species, the structural basis of these asymmetries is largely unknown. We now report that due to an asymmetry of commissural projections in the pigeon the left nucleus rotundus of the ascending tectofugal visual system predominantly represents inputs from both eyes while the right nucleus rotundus mainly represents the contralateral left eye. We suggest that a comparable organization exists for several asymmetries in humans. A representation of both hemifields can provide the dominant hemisphere with direct access to all stimulus features when objects cross the vertical meridian.

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.

The differential distribution of AMPA-receptor subunits in the tectofugal system of the pigeon

The tectofugal system of the pigeon was examined for the distribution of several glutamate-receptor subunits (AMPA Glu R1, Glu R2/3, Glu R4) and the calcium binding protein parvalbumin. With respect to the different antigens, a heterogeneous distribution was observed. Within the optic tectum, the Glu R1 like immunoreactivity was limited to the layers 2-5, 9, 10, and sparsely in layer 13, whereas the antibody to Glu R2/3 stained cell bodies in layers 9, 10, and very heavily in layer 13. In the rotundus only the Glu R4 antigen was expressed, while within the ectostriatal complex a large number of Glu R2/3 and a smaller contingent of Glu R4 positive neurons were stained. Quantitative analysis proved significant heterogeneities of these antigens in the mesencephalic as well as the diencephalic centre of the tectofugal pathway. The number of Glu R2/3 positive neurons undergoes a two-fold increase from the dorsal to the ventral lamina 13 of the optic tectum. Alterations in the amount of immunoreactive neurons were also observed within the rotundus, since the number of Glu R4 positive cells decreased from dorsal to ventral. Morphological differences and their correlation with functional specializations in visual information processing are discussed.

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 receptor architecture of the pigeons’ nidopallium caudolaterale: an avian analogue to the mammalian prefrontal cortex

The avian nidopallium caudolaterale is a multimodal area in the caudal telencephalon that is apparently not homologous to the mammalian prefrontal cortex but serves comparable functions. Here we analyzed binding-site densities of glutamatergic AMPA, NMDA and kainate receptors, GABAergic GABAA, muscarinic M1, M2 and nicotinic (nACh) receptors, noradrenergic α1 and α2, serotonergic 5-HT1A and dopaminergic D1-like receptors using quantitative in vitro receptor autoradiography. We compared the receptor architecture of the pigeons’ nidopallial structures, in particular the NCL, with cortical areas Fr2 and Cg1 in rats and prefrontal area BA10 in humans. Our results confirmed that the relative ratios of multiple receptor densities across different nidopallial structures (their “receptor fingerprints”) were very similar in shape; however, the absolute binding densities (the “size” of the fingerprints) differed significantly. This finding enables a delineation of the avian NCL from surrounding structures and a further parcellation into a medial and a lateral part as revealed by differences in densities of nACh, M2, kainate, and 5-HT1A receptors. Comparisons of the NCL with the rat and human frontal structures showed differences in the receptor distribution, particularly of the glutamate receptors, but also revealed highly conserved features like the identical densities of GABAA, M2, nACh and D1-like receptors. Assuming a convergent evolution of avian and mammalian prefrontal areas, our results support the hypothesis that specific neurochemical traits provide the molecular background for higher order processes such as executive functions. The differences in glutamate receptor distributions may reflect species-specific adaptations.

Visual-field-specific heterogeneity within the tecto-rotundal projection of the pigeon

The organization of the tecto‐rotundal projection of the pigeon was investigated by means of anterograde and retrograde tracing techniques. Besides the known organization in tecto‐rotundal connectivity, this study additionally demonstrates major variations in the ascending projections of different tectal subfields. We show that the ventral tectum opticum (TO) has significantly more projections onto the nucleus rotundus (Rt) than dorsal tectal areas. This difference coincides with differential innervation densities of afferent fibres within rotundal subregions. While ventral tectal efferents project onto the ventral and central Rt, dorsal tectal efferents mainly arborize within limited areas between the central Rt and its dorsal cap, the nucleus triangularis. Thus, the ventral TO, representing the lower and frontal field of view, exhibits a quantitatively and spatially enhanced projection onto the Rt, as compared with the dorsal TO. The data presented here demonstrate a visual field‐dependent projection pattern of ascending tectal outputs onto different rotundal domains. The data are consistent with behavioural studies, demonstrating tectofugal lesions to suppress visual stimulus analysis mainly within the frontal field of view.

Cytochrome oxidase activity reveals parcellations of the pigeon's ectostriatum.

The endogenous cytochrome oxidase activity of the pigeon’s ectostriatum, the primary telencephalic structure of the tectofugal visual pathway, was histochemically demonstrated and a heterogeneous distribution of the reaction product was observed. In cross-sections the medial, central and ventrolateral parts of the ectostriatum showed high levels of activity while the centroventral and dorsolateral ectostriatum remained weakly labelled. Only slight left-right and interindividual variations were found in the pattern of labelling. These data demonstrate for the first time anatomical subdivisions within the ectostriatal core and open the possibility of functional parcellations within this structure.

Electrophysiological and anatomical evidence for a direct projection from the nucleus of the basal optic root to the nucleus rotundus in pigeons.

A direct projection of the nucleus of the basal optic root (nBOR) onto the nucleus rotundus (Rt) in the pigeon would link the accessory optic system to the ascending tectofugal pathway and could thus combine self- and object-motion processes. In this study, injections of retrograde tracers into the Rt revealed some cells in central nBOR to project onto the ipsilateral Rt. Contrary, injections into the diencephalic component of the ascending thalamofugal pathway resulted in massive labeling of neurons in dorsal nBOR. Single unit recordings showed that visual nBOR units could be activated by antidromic stimulation through the Rt. Successful collision tests applied to nBOR cells revealed that the connection between nBOR and Rt is direct. These data provide strong evidence for a direct and differential projection of nBOR subcomponents onto the thalamic relays of the two ascending visual pathways.

Catecholaminergic and dopamine-containing neurons in the spinal cord of pigeons: an immunohistochemical study

Within the different species belonging to the vertebrate radiation, catecholaminergic elements of the spinal cord present a partly conservative, partly variable pattern. Unfortunately, the overall picture is far from clear since the situation for birds is largely obscure. Therefore, we examined the distribution of dopamine (DA)- and tyrosine hydroxylase (TH)-positive cells and fibers in the spinal cord of the adult pigeon by immunohistochemistry. TH-immunoreactive cells were located within two restricted areas. One group of cells with multipolar shape was located in laminae VI and VII, close to the white-gray border. These cells were more frequently found at rostral and caudal levels while being scarce at cervical-thoracic levels. The second group of cells was located in lamina VIII surrounding the central canal. These cells were bipolar in shape and were found ventrally and laterally to the central canal, with most of them contacting the lumen of the canal through a separate process. The TH-immunoreactive fibers were distributed in both the gray and the white matter. In the gray matter, they were mainly distributed around the central canal (lamina VIII), in the ventral horn close to the border of laminae VII-IX and in the lateral part of the dorsal horn in laminae II-VI. In the white matter the fibers were present in the lateral columns running longitudinal to the main axis. DA-immunoreactive cells were also located within two restricted areas, closely matching the distribution of TH-immunopositive ones. Additionally, the DA-immunoreactive cells had the same shape as the TH-immunoreactive cells, as bipolar neurons contacted the central canal and multipolar ones were located in the laminae VI and VII. Also the distribution of DA- and TH-immunoreactive fibers roughly matched. Both, DA-immunoreactive cells and fibers were scarcer than TH-immunoreactive ones. This finding suggests that the catecholaminergic system in the spinal cord consists of DA-immunoreactive cells as well as other catecholaminergic cells.