Transneuronal transport of [³H]proline within the visual system of the grey squirrel

Vision is the dominant sense in primates. This article attempts to reconstruct a reasonable scenario as to how parallel visual pathways might have evolved in primates by comparing key factors that might distinguish this group evolutionarily. The focus is on visual information channels from the eye through the lateral geniculate nucleus (LGN) of the thalamus to cortex since these pathways may have become uniquely specialized in primate evolution. We defend the position that magnocellular (M) and parvocellular (P) retinogeniculocortical pathways are homologous across primates and therefore probably existed in the mammalian common ancestor of primates. Whether homologues to these visual pathways can be found in extant mammals remains controversial, but evidence suggests that functionally similar pathways can be identified in a range of mammals. Even for the less well-researched koniocellular (K) pathway, data exist suggesting an early evolutionary history. Only among primates, however, is the evidence strong enough to support homology. We also present data suggesting that the common ancestor to primates was dichromatic and that early primates may even have been diurnal given the existence of genes for at least two cone types in all primates. We also review evidence for homologies between ocular dominance pathways and other properties. In addition, we review evidence for the evolutionary history of cortical hierarchies of visual areas and conclude that only a few areas can be considered homologous across primates and even fewer across mammals. In the final section, we provide a summary and also outline questions that should be addressed in order to arrive at more definitive conclusions concerning the evolution of parallel visual pathways. We also outline some practical strategies for answering some of these questions.

Transneuronal transport of biotinamide was observed following intracellular injection of biotinamide into rat jaw-muscle spindle afferent axons. Microelectrodes were advanced into the mesencephalic nucleus of the trigeminal nerve where jaw-muscle spindle afferent axons were identified by their increased firing during stretching of the jaw-elevator muscles. Biotinamide (Neurobiotin) was then injected into individual axons and the animals were maintained under anesthesia for 2−6 h. The animals were then killed via an overdose of anesthetic and the brainstem was processed histochemically. Biotinamide-filled axon collaterals and terminals were readily visible in the trigeminal motor nucleus, the trigeminal sensory nuclei, and adjacent reticular formation. In addition to these intracellularly stained axons, two to five neurons per animal (total of 36 in eight rats) were observed with a homogenous gray reaction product distributed throughout their somata, proximal, and secondary dendrites. These neurons ranged in size from small (8–20 μm, n = 26) to medium-sized (<30 μm, n = 10) and were closely apposed by numerous (up to 20) biotinamide-stained spindle afferent boutons. Most of these neurons (n = 22) were located in the dorsomedial portion of the spinal trigeminal subnucleus interpolaris (Vi) 2.5−4.5 mm caudal to the intra-axonal injection site. Electron microscopic analysis in two rats suggests that the transneuronal biotinamide labeling occurred predominately through asymmetric, axodendritic synapses between biotinamide-filled axon terminals and Vi neuronal dendrites. Although recent in vitro studies have reported that biotinamide permeates through gap junctions, in this study we found no evidence of biotinamide traversing the gap junctions which exist between trigeminal mesencephalic nucleus (Vme) neuronal somata. These results demonstrate that biotinamide can occasionally be transneuronally transported presumably via synapses; further information is needed to explain the seemingly sporadic nature of this transport.

The ipsilateral retinal projections and laminations of the dorsal lateral geniculate nucleus (LGNd) were studied in the eastern chipmunk (Tamias sibiricus asiaticus). From cyto-, myelo- and chemoarchitectures the LGNd was divided into the ventromedial and dorsolateral parts. Anterograde axonal transport of wheat germ agglutinated horseradish peroxidase (WGA-HRP) and Fink-Heimer staining after unilateral eye removal both indicated that the ipsilateral projection terminates in lamina 2 of the ventromedial part and in lamina 3b of the dorsalateral part. The remaining laminas, lamina 1 of the ventromedial part and laminas 3a and 3c of the dorsolateral part, receive afferents from the contralateral retina. It was suggested that laminas 1 and 2 of the chipmunk's LGNd correspond to laminas A and A1 of the cat's LGNd, and the lamina 3 complex to its lamina C complex.

The projection of the retinal ganglion cells to the terminal nuclei of the accessory optic system has been re-examined in the albino rat. After intravitreal injection of [³H]eucine the contralateral and ipsilateral terminal nuclei were labeled. This complete ipsilateral projection in the rat has, of yet, not been documented.

Anterograde autoradiographic experiments reveal connectional specificity between the dorsal lateral geniculate (LGN) laminae and striate cortical layers in a rodent, the gray squirrel (Sciurus carolinensis). Our data indicate that although the geniculostriate projection does not segregate right and left eye information within layer IV, geniculate projections to this layer are tightly organized such that particular cortical substrata receive input from specific LGN layer(s). Preliminary data suggest that geniculate layers 1 and 2 of the LGN project to a central zone of layer IV. In contrast, the layer 3 complex projects densely to a dorsal and ventral tier in layer IV, as well as to layer VI and the supragranular laminae. It is speculated that the input to supragranular layers arises from cells within layer 3c, which in turn, have been shown to receive input from the stratum griseum superficiale of the superior colliculus. It is argued that this tecto-geniculo-supragranular cortical pathway might convey W-cell information, as has been suggested for other species.