Spatial organization of the pigeon tectorotundal pathway: An interdigitating topographic arrangement

Abstract

The retinotectofugal system is the main visual pathway projecting upon the telencephalon in birds and many other nonmammalian vertebrates. The ascending tectal projection arises exclusively from cells located in layer 13 of the optic tectum and is directed bilaterally toward the thalamic nucleus rotundus. Although previous studies provided evidence that different types of tectal layer 13 cells project to different subdivisions in Rt, apparently without maintaining a retinotopic organization, the detailed spatial organization of this projection remains obscure. We reexamined the pigeon tectorotundal projection using conventional tracing techniques plus a new method devised to perform small deep-brain microinjections of crystalline tracers. We found that discrete injections involving restricted zones within one subdivision retrogradely label a small fraction of layer 13 cells that are distributed throughout the layer, covering most of the tectal representation of the contralateral visual field. Double-tracer injections in one subdivision label distinct but intermingled sets of layer 13 neurons. These results, together with the tracing of tectal axonal terminal fields in the rotundus, lead us to propose a novel "interdigitating" topographic arrangement for the tectorotundal projection, in which intermingled sets of layer 13 cells, presumably of the same particular class and distributed in an organized fashion throughout the surface of the tectum, terminate in separate regions within one subdivision. This spatial organization has significant consequences for the understanding of the physiological and functional properties of the tectofugal pathway in birds.

A Dissociation of Motion and Spatial-Pattern Vision in the Avian Telencephalon: Implications for the Evolution of “Visual Streams”

“…Given that the nRT contains several distinct areas on the basis of neurochemistry, cytoarchitecture, tectal innervation, and physiology Benowitz and Karten, 1976;Revzin, 1979;Watanabe et al, 1985;Martinez-de-la-Torre et al, 1990;Wang et al, 1993;Mpodozis et al, 1996;Marin et al, 2003) and that the topographic nRT-Ec projection may be quite precise (Husband and Shimizu, 1999;Laverghetta and Shimizu, 2003), it is proba- Figure 4. Correlation between performance and the extent of the lesion in Ec.…”

“…5, middle). The deep layers in the tectum project to caudal nRT, whereas the superficial layers project to rostral nRT (Benowitz and Karten, 1976;Marin et al, 2003); the caudal and rostral nRT project to the caudal and rostral Ec, respectively (Benowitz and Karten, 1976;Husband and Shimizu, 1999;Laverghetta and Shimizu, 2003). Ec projects differentially to areas of the telencephalon: the caudal and rostral Ec project to the neostriatum intermediale (NIL) and neostriatum frontale (NFL), respectively (Husband and Shimizu, 1999).…”

“…On the basis of neurochemistry, cytoarchitecture, tectal innervation, and physiology, nRT has been divided into several subnuclei (Benowitz and Karten, 1976;Martinez-dela-Torre et al, 1990;Mpodozis et al, 1996;Marin et al, 2003). Early electrophysiological studies showed that the majority of cells in nRT were motion sensitive (Revzin, 1979).…”

Auditory and Multisensory Responses in the Tectofugal Pathway of the Barn Owl

“…These cells possess large dendritic arbors and have been shown to have large visual receptive fields with high sensitivity to moving visual stimuli (Luksch et al, 1998). Interestingly, a single site in nRt receives inputs from TGCs that are evenly distributed throughout the OT (Marín et al, 2003). This arrangement implies a strong reduction of spatial sensitivity from the superficial and intermediate layers of the OT to nRt.…”

Attentional Capture? Synchronized Feedback Signals from the Isthmi Boost Retinal Signals to Higher Visual Areas

“…Tectal ganglion cells (TGCs) in deeper layers pool this precise retinotopy and project to the thalamic nucleus rotundus ( Fig. 1 A, B) (Benowitz and Karten, 1976;Karten et al, 1997;Luksch et al, 1998;Hellmann and Gü ntü rkü n, 2001;Luksch et al, 2001;Marín et al, 2003), resulting in large receptive fields (RFs), which typically would contain several stimuli simultaneously.…”