Retinal ganglion cells projecting to the nucleus of the optic tract and the dorsal terminal nucleus of the accessory optic system in macaque monkeys

Abstract

Using classical neuroanatomical retrograde tracing methods we investigated the retinal ganglion cells projecting to the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic system (NOT-DTN) in macaque monkeys. Our main aim was to quantify the strength of the projection from the ipsilateral retina to the NOT-DTN. We therefore examined the number, distribution, and soma size of retinal ganglion cells involved in this projection. Electrophysiologically controlled small injections into the NOT-DTN revealed a clearly bilateral retinal projection originating mainly from the central retina but also involving peripheral retinal regions. Labelled cells were found nasally in the contralateral retina and temporally in the ipsilateral retina with some overlap in the fovea. The projection from the ipsilateral retina was 36-43% of that from the contralateral retina. On average, only 1-6% of the local population of ganglion cells projected to the NOT-DTN. Small soma size and large dendritic fields imply that in monkey rarely encountered, 'specialized' ganglion cells provide the direct retinal input to the accessory optic system (AOS). These results are discussed with respect to the symmetry of monocular horizontal optokinetic nystagmus (OKN) in primates.

Visual Pathway for the Optokinetic Reflex in Infant Macaque Monkeys

“…Lesion studies in primates demonstrate the relevance of striate and extrastriate visual cortical areas for unperturbed slow eye movements and symmetric mhOKN (e.g., Ter Braak and Van Vliet, 1963;Lynch and McLaren, 1983;Zee et al, 1987;Dürsteler and Wurtz, 1988). As we failed to reveal a cortical input to the NOT-DTN at P9, binocularity in the NOT-DTN up to this age should indeed originate from the direct projections of retinal ganglion cells from both eyes (Ballas et al, 1981;Kourouyan and Horton, 1997;Telkes et al, 2000). However, already at P12 and P14, we could convincingly demonstrate a direct cortical projection to the NOT-DTN arising from V1 and even more strongly from MT which, however, did not increase binocular balance at once, i.e., a large proportion of neurons was still dominated by the contralateral eye.…”

Directional Asymmetry of Neurons in Cortical Areas MT and MST Projecting to the NOT-DTN in Macaques

“…The data for the present investigation were accu-mulated over the last 10 yr in 12 hemispheres of adult macaque monkeys of both sexes, 6 Macaca mulatta and 4 M. fascicularis, some of which prior to this terminal experiment were involved in other studies. Brain tissue from these animals served for anatomical studies (Distler and Hoffmann 2001;Telkes et al 2000).…”

“…However, it has been a paradox so far why lesions of various cortical areas lead to severe direction selective deficits in slow eye movements, and the question about the neuronal basis of this so-called directional asymmetry of the smooth pursuit and optokinetic system has intrigued neuroscientists for some time (e.g., Barton et al 1996;Braddick 1996;Dürsteler and Wurtz 1988;Heide et al 1996;Lynch and McLaren 1983;Sharpe 1993, 1995;Ter Braak and Van Vliet 1963;Thurston et al 1988;Tusa et al 1989;Wood et al 1973;Zee et al 1987). In normal cats, monkeys, and humans, monocularly as well as binocularly elicited slow eye movements are largely equivalent during clockwise and counterclockwise stimulation (symmetrical OKN).…”

Development of the Optokinetic Response in Macaques

“…Due to the distinct retinal decussation pattern, in primates this retinal projection is much more bilateral, the ipsilateral projection reaching about 40% of the contralateral projection. 1 This bilateral retinal projection is present at birth. 2 Experiments in wallabies strongly indicate that the retina imprints the behaviorally relevant direction selectivity on the retinal slip neurons: rotation of the anlage of the eye causes a corresponding rotation of the preferred direction of retinal slip neurons.…”