The accessory optic system of Rana pipiens: Neuroanatomical connections and intrinsic organization

Abstract

The accessory optic system of Rana pipiens was investigated by autoradiographic, horseradish peroxidase, and Golgi techniques, revealing a complexity of neuroanatomical organization previously unrecognized. Retinal afferents project to the nucleus of the basal optic root (nBOR) via a primary bundle and more diffuse, medial bundle of optic axons, both of which contain large- and small-diameter fibers. At least six types of retinal ganglion cell contribute to the basal optic root (BOR), including giant ganglion cells, two intermediate-sized ganglion cell types, small ganglion cells, and two types of displaced ganglion cell. The major retinal projection is contralateral, but a small, ipsilateral component also exists. Afferents from neurons which are postsynaptic to the thalamic retinal terminal fields also reach nBOR. Four distinct cell types were identified within the terminal field of nBOR: stellate neurons (63%), amacrine cells (19%), elongate neurons (14%), and large ganglionic neurons (4%). Both stellate and amacrine cells appear to be intrinsic neurons, while elongate and ganglionic neurons constitute the efferent neuron population of nBOR. In addition, cells which lie medial to the terminal field, pyriform and commissural neurons, send dendrites into nBOR. Pyriform neurons project to the nucleus of the medial longitudinal fasciculus (nMLF) and cranial nerve nuclei III and IV, while commissural neurons project to the contralateral nBOR. Large reticular neurons of the nMLF also send dendrites into nBOR. Efferent projections from nBOR were observed in the large-celled pretectal nucleus and in nucleus lateralis profundus. A second major projection originates from the peri-nBOR region and is associated with the oculomotor system and with the nMLF. Efferent projections from the nMLF to the vestibular nuclei and to the rostral spinal cord were also observed, as well as projections which reach the brainstem from the large-celled pretectal nucleus, the posterior thalamic and anterior mesencephalic central gray.

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

“…Studies also showed the presence of a basic accessory optic system in amphibians (frog: Montgomery et al, 1981;Lazar, et al, 1983;salamanders: Riss et al, 1963;Jakway and Riss, 1972;Gruberg, 1973) and reptiles (turtles: Bass andNorthcutt, 1981, Martin et al, 2003;lizards: Butler and Northcutt, 1971;snakes: Rio et al, 1983). Among birds, the pigeon AOS is well developed and consists of a BOR whose fibers terminate in principal (nBORp), dorsal (nBORd) and lateral divisions (nBORl) of the nBOR all found in the ventral midbrain tegmentum (VTA).…”

“…This scheme was introduced by Hayhow and colleagues (see Hayhow, 1959Hayhow, , 1966Hayhow et al, 1960). Among non-mammalian species, the retinofugal fibers to the nBOR were described in amphibians, reptiles and birds as arising from a distinct set of retinal ganglion cells, the displaced ganglion cells Reiner et al, 1979;Fite et al, 1981;McKenna and Wallman, 1985). These fibers project via the basal optic root (BOR) to the nucleus of the basal optic root (nBOR) located in the midbrain tegmentum.…”

“…Among birds, the pigeon AOS is well developed and consists of a BOR whose fibers terminate in principal (nBORp), dorsal (nBORd) and lateral divisions (nBORl) of the nBOR all found in the ventral midbrain tegmentum (VTA). For details about the nonmammalian AOS, the interested reader should consult articles by, e.g., Karten et al, 1977;Mai, 1978;Reiner et al, 1979;Brecha et al, 1980;Wallman et al, 1981;Fite et al, 1981;Fite, 1985. Mammalian species: Data pertaining to the AOS tracts and terminal nuclei of nontherian mammals (monotremes) are important in an evolutionary sense. The egg-laying, monotremes, echidna and duckbilled platypus, are the sole surviving representatives of nontherian mammals and are highly specialized for their mode of life.…”

Monocular and Binocular Optic Inputs to Salamander Pretectal Neurons: Intracellular Recording and HRP Labelling Study

“…These neurons with their efferents via the medial longitudinal fasciculus are si milar to cells of the nucleus of the medial longitudinal fasciculus described in frogs [Montgomery et al, 1981], They, therefore, might not represent pretectal neurons in a strict sense. However, in frogs these cells lack dendrites in the pretectum and are mostly associated with neurons scattered in the tegmentum of that region.…”

A 'Physiological' Model for the Salamander Horizontal Optokinetic Reflex

“…Looking upon the salamander brain in a simplistic way, it may be proposed that a recurrent network is built up by the perinBOR and the nMLF neural system, which has been identified in the frog teg mentum [Montgomery et al, 1981] and which also exists in the salamander [Naujoks-Manteuffel and Manteuffel, in prep aration], Neuronal elements of the circuit may be characterized in intracellular re cording experiments by means of their theoretically expected response properties to single and multiple pulses.…”