Projections from visual areas of the cerebral cortex to pretectal nuclear complex, terminal accessory optic nuclei, and superior colliculus in macaque monkey

Abstract

The purpose of this study was to analyze the projections from visually related areas of the cerebral cortex of rhesus monkey to subcortical nuclei involved in eye-movement control; i.e., the pretectal nuclear complex, the terminal nuclei of the accessory optic system (AOS), and the superior colliculus (SC). The anterograde tracer 3H-leucine was pressure injected bilaterally into the cortex of six monkeys (for a total of 12 cases) involving the primary visual cortex (area 17); the medial prestriate cortex (medial 18/19); dorsomedial area 19; the caudal portion of the cortex of the superior temporal sulcus, upper bank (cytoarchitectural area OAa) and lower bank (area PGa); the lower bank of the caudal lateral intraparietal sulcus (area POa); and the inferior parietal lobule (area 7). The results revealed that the pretectal nucleus of the optic tract received inputs from medial prestriate cortex, dorsomedial part of area 19, OAa, and PGa. The posterior pretectal nucleus received sparse projections from area 7 and the cortex lining the intraparietal sulcus (dorsomedial part of area 19 and POa). The pretectal olivary nucleus was targeted by neurons in cortex of dorsomedial area 19, and the anterior pretectal nucleus was targeted by neurons in both dorsomedial 19 and area 7. The nuclei of the AOS (dorsal terminal; lateral terminal; and interstitial nuclei of the superior fasciculus, posterior and medial fibers) received projections exclusively from areas OAa and PGa. Furthermore, in one case with PGa injection, the medial terminal nucleus, dorsal portion, was also labeled. The visual cortical areas studied projected differentially upon the SC laminae. The primary visual area 17 projected only to the superficial laminae, i.e., stratum zonale (SZ), stratum griseum superficiale (SGS), and stratum opticum (SO). On the other hand, the medial portion of the prestriate cortex and caudal OAa and PGa targeted the superficial and intermediate laminae, i.e., SZ, SGS, SO, and stratum griseum intermediale (SGI), whereas caudal area POa projected primarily to the intermediate layer SGI. Rostral area 7 (mainly 7b) neurons terminated in the stratum album intermediale (SAI); no SC terminals were found in a case in which caudal area 7 (mainly 7a) was injected.

The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function

“…Projections to the LTN appear to arise selectively from these visual areas (Spatz and Tigges., 1973;Maioli et al, 1989;Lui et al, 1995). Other authors (Boussaoud et al, 1992) found projections to the LTN in one case with a tracer injection involving area FST (fundus of the superior temporal sulcus), which is also involved in visual motion detection (see, e.g., Vanduffel et al, 2001).…”

“…The latter is of paramount importance in dealing with weak projections to small structures such as the AOS. The primary visual cortex (V1) was found to project to the LTN (the most conspicuous AOS nucleus in primates) in some studies (Campos-Ortega and Hayhow, 1972), but not in others (Maioli et al, 1989;Lui et al, 1995). These inconsistencies suggest the possibility that only specific retinotopic regions of V1 (corresponding to the representation of the vertical meridian) may be responsible for this connection .…”

“…Further, in rodents and lagomorphs there is no visual cortical projection to the AOS nuclei whereas there is to the NOT (e.g., rabbit: Giolli and Guthrie, 1971;rat: Lui et al, 1994). It is true that in primates, the accessory optic nuclei and NOT both receive input from visual and oculomotor-related areas of cortex Distler and Hoffmann, 2001), viz., from the cortex lining the superior temporal sulcus in macaque monkey; but it is the NOT alone that is targeted by cortical neurons arising from certain other visual areas (VIP, V3, V3a and V4 and dorsomedial area 19: see Lui et al, 1995). Moreover, the AOS nuclei contain large numbers of CGRP immunoreactive somata and axons terminals compared to the NOT, which contains neither CGRP-positive cells or terminals (Ribak et al, 1997).…”

A competitive integration model of exogenous and endogenous eye movements

“…Many theories assume that the site of this saccade map is the intermediate layers of the superior colliculi (SC) 1 (Godijn and Theeuwes 2002;Munoz et al 2000;Trappenberg et al 2001), perhaps together with other oculomotor areas (e.g., the frontal eye fields, Munoz and Schall 2003). The SC integrate input from many cortical areas, such as the frontal eye fields (FEF), the supplementary eye fields, the posterior parietal cortex, dorsolateral prefrontal cortex (DLPFC), and occipital visual areas (Lock et al 2003;Lui et al 1995;Munoz 2002). They send the result of this integration process to the cerebellar and brainstem premotor circuitry where the eye movement is programmed (Moschovakis 1996).…”

The effect of pupil size on binocular summation at suprathreshold conditions

“…The nucleus of this nerve, located in the midbrain, has cortical projections to occipito-parietal areas. [4][5][6] Pupils react by contracting in response to light and near viewing, and by dilating in response to darkness and far viewing. 4,[7][8][9] Moreover, pupil size is smaller in binocular than in monocular vision.…”