Organization of geniculocortical projections in turtles: Isoazimuth lamellae in the visual cortex

Abstract

The projection from the dorsal lateral geniculate complex to the visual cortex in Pseudemys and Chrysemys turtles was examined by using the anterograde transport of horseradish peroxidase (HRP) in vitro and the retrograde transport of HRP in vivo. In vitro HRP injections into the lateral forebrain bundle were used to fill geniculocortical axons anterogradely, which were then analyzed in cortical wholemount preparations. Geniculocortical axons gain access to the visual cortex along its entire rostral-caudal extent. They course in slightly curved trajectories for up to 2 mm from the lateral edge of the cortex through both the lateral (or pallial thickening) and medial parts of Desan's cortical area D2. Single axons are of fine caliber. They tend to cross each other and sometimes branch in the pallial thickening, but are generally unbranched in the medial part of D2. They bear small, fusiform varicosities at irregular intervals along their lengths. Although axons show small variations in the number of varicosities per 100 microns segment, no consistent variation in varicosity number as a function of distance could be detected. These results indicate that geniculocortical axons project to the visual cortex in an orderly pattern. The retrograde transport experiments provide some clue as to the significance of this pattern. Small, ionotophoretic injections of HRP in the visual cortex retrogradely labeled neurons in the dorsal lateral geniculate complex. Injections in the rostral visual cortex retrogradely labeled neurons in the caudal pole of the geniculate complex. Injections at progressively more caudal loci within the visual cortex labeled neurons at progressively more rostral loci within the geniculate complex. Thus, there is a representation of the rostral-caudal axis of the geniculate complex along the caudal-rostral axis of the visual cortex. Consistent with the anterograde transport experiments that showed individual geniculocortical axons coursing through both lateral and medial parts of the visual cortex, HRP injections restricted to the medial edge of the visual cortex retrogradely labeled neurons along the entire dorsal-ventral axis of the geniculate complex at the appropriate rostral-caudal position. The neurophysiological studies of Mazurskaya ('72: J. Evol. Biochem. Physiol. 8:550-555; respond to a small, moving stimulus anywhere in visual space, implying a convergence of inputs from all points in visual space somewhere along the retinogeniculocortical pathway. The experiments reported here suggest a convergence in the geniculocortical projections of information along the vertical meridians, or azimuth lines, of visual space onto neurons lying along lateral to medial transects through the visual cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Micro-, Meso- and Macro-Dynamics of the Brain

“…Layer 3 contains basal dendrites of pyramidal cells, corticofugal and local axons, some interneurons and a few deep pyramidal neurons in PCx (Neville and Haberly 2004;Ulinski 1990). Incoming afferents to PCx run through the lateral olfactory tract (LOT; Sosulski et al 2011); those to DCx run through the lateral forebrain bundle (LFB; Mulligan and Ulinski 1990). These input fibers fan out below the pial surface and make en-passant synapses on cortical neurons within the distal 50-100 μm of layer 1 (Haberly and Behan 1983;Smith et al 1980).…”

“…Although this does not rule out the possibility of some fine-scale topographical mapping of OB projections (e.g., mitral vs. tufted cell projections) (Igarashi et al 2012), it is now accepted that the glomerular clustering of olfactory receptor cells axons in OB is entirely discarded at the level of PCx (Wilson and Sullivan 2011). In DCx, early tracing studies from Ulinski and colleagues suggested that the visual field is projected onto the rostro-caudal axis of DCx in the form of iso-azimuth lamellae covering the naso-temporal dimension of the visual field (Mulligan and Ulinski 1990;Ulinski and Nautiyal 1988). Such a mapping of projections still awaits physiological confirmation and fine thalamocortical projection tracing.…”

“…Hence, the balance between afferent and associational connectivity decreases along the rostro-caudal and latero-medial (or ventro-dorsal) axes (Mulligan and Ulinski 1990;Haberly 2001;Wilson and Sullivan 2011;Hagiwara et al 2012;Cosans and Ulinski 1990). PCx is subdivided into anterior and posterior regions, which differ not only in the density of afferent vs. associational fibers (Haberly 2001) but also in the properties of odor-evoked responses (Litaudon et al 2003;Kadohisa and Wilson 2006).…”

Dendritic Properties of Turtle Pyramidal Neurons

“…In mammals it survives in both the piriform cortex and the hippocampal formation, often termed "archicortex" or "paleocortex." In turtles (and other reptiles) the three-layered pallium processes not only olfactory but also other sensory information relayed via the thalamus (Desan 1984;Hall and Ebner 1970;Mulligan and Ulinski 1990). There is a broad range of evidence establishing that the more elaborate sixlayered neocortex was derived from the pallium (e.g., Mulligan and Ulinski 1990;Reiner 2000).…”

“…In turtles (and other reptiles) the three-layered pallium processes not only olfactory but also other sensory information relayed via the thalamus (Desan 1984;Hall and Ebner 1970;Mulligan and Ulinski 1990). There is a broad range of evidence establishing that the more elaborate sixlayered neocortex was derived from the pallium (e.g., Mulligan and Ulinski 1990;Reiner 2000). In particular, there is evidence that projections onto the dendrites of turtle pyramidal neurons from other cortical and subcortical regions are more laminar and organized than in mammalian pyramidal neurons (Desan 1984;Hall and Ebner 1970;Mulligan and Ulinski 1990;Smith et al 1980).…”