Research over the past two decades in mammals, especially primates, has greatly improved our understanding of the afferent and efferent connections of two retinorecipient pretectal nuclei, the nucleus of the optic tract (NOT) and the pretectal olivary nucleus (PON). Functional studies of these two nuclei have further elucidated some of the roles that they play both in oculomotor control and in relaying oculomotor-related signals to visual relay nuclei. Therefore, following a brief overview of the anatomy and retinal projections to the entire mammalian pretectum, the connections and potential roles of the NOT and the PON are considered in detail. Data on the specific connections of the NOT are combined with data from single-unit recording, microstimulation, and lesion studies to show that this nucleus plays critical roles in optokinetic nystagmus, short-latency ocular following, smooth pursuit eye movements, and adaptation of the gain of the horizontal vestibulo-ocular reflex. Comparable data for the PON show that this nucleus plays critical roles in the pupillary light reflex, light-evoked blinks, rapid eye movement sleep triggering, and modulating subcortical nuclei involved in circadian rhythms.

The pretectum: connections and oculomotor-related roles.

The optokinetic response (OKR) is a stereotyped
eye movement in response to movement in he surround. The OKR serves to stabilize the visual image on the retina, and allows for high resolution vision. Due to its high selection value, all vertebrates display this basic behavior. Here, we review the properties of the OKR with a focus on the zebrafish, including methodological aspects of measuring eye movements in small larvae. The genetic amenabilities of the zebrafish model permit the use of this reflexive behavior in genetic screens. Such approaches have led to the isolation of mutant strains with specific defects in the visual pathway. In addition to the use of the OKR as a screening assay, mutations with characteristic abnormalities in the execution of this behavior will enable the analysis of sensory-motor control in great detail. A case in point is the belladonna mutation, where an axonal misrouting effect at the optic chiasm leads to a reversed OKR with a number of interesting properties.

The optokinetic response in zebrafish and its applications

The accessory optic system (AOS) is formed by a series of terminal nuclei receiving direct visual information from the retina via one or more accessory optic tracts. In addition to the retinal input, derived from ganglion cells that characteristically have large receptive fields, are direction-selective, and have a preference for slow moving stimuli, there are now well-characterized afferent connections with a key pretectal nucleus (nucleus of the optic tract) and the ventral lateral geniculate nucleus. The efferent connections of the AOS are robust, targeting brainstem and other structures in support of visual-oculomotor events such as optokinetic nystagmus and visual-vestibular interaction. This chapter reviews the newer experimental findings while including older data concerning the structural and functional organization of the AOS. We then consider the ontogeny and phylogeny of the AOS and include a discussion of similarities and differences in the anatomical organization of the AOS in nonmammalian and mammalian species. This is followed by sections dealing with retinal and cerebral cortical afferents to the AOS nuclei, interneuronal connections of AOS neurons, and the efferents of the AOS nuclei. We conclude with a section on Functional Considerations dealing with the issues of the response properties of AOS neurons, lesion and metabolic studies, and the AOS and spatial cognition.

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

Almost all vertebrates are capable of recognizing biologically relevant stimuli at or shortly after birth, and in some phylogenetically ancient species visual object recognition is exclusively innate. Extensive and detailed studies of the anuran visual system have resulted in the determination of the neural structures and pathways involved in innate prey and predator recognition in these species [Behav. Brain Sci. 10 (1987) 337; Comp. Biochem. Physiol. A 128 (2001) 417]. The structures involved include the optic tectum, pretectal nuclei and an area within the mesencephalic tegmentum. Here we investigate the structures and pathways involved in innate stimulus recognition in avian, rodent and primate species. We discuss innate stimulus preferences in maternal imprinting in chicks and argue that these preferences are due to innate visual recognition of conspecifics, entirely mediated by subtelencephalic structures. In rodent species, brainstem structures largely homologous to the components of the anuran subcortical visual system mediate innate visual object recognition. The primary components of the mammalian subcortical visual system are the superior colliculus, nucleus of the optic tract, anterior and posterior pretectal nuclei, nucleus of the posterior commissure, and an area within the mesopontine reticular formation that includes parts of the cuneiform, subcuneiform and pedunculopontine nuclei. We argue that in rodent species the innate sensory recognition systems function throughout ontogeny, acting in parallel with cortical sensory and recognition systems. In primates the structures involved in innate stimulus recognition are essentially the same as those in rodents, but overt innate recognition is only present in very early ontogeny, and after a transition period gives way to learned object recognition mediated by cortical structures. After the transition period, primate subcortical sensory systems still function to provide implicit innate stimulus recognition, and this recognition can still generate orienting, neuroendocrine and emotional responses to biologically relevant stimuli.

Innate visual object recognition in vertebrates: some proposed pathways and mechanisms.

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 arec 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, 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. © 1995 Wiley-Liss, Inc.

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

The primary goal of this study was to determine whether the striate cortex (Oc 1) of the guinea pig projects to the pretectal nucleus of the optic tract (NOT), the first postretinal station of the horizontal optokinetic pathway, and, if so, to analyze the anatomical organization of this cortico-NOT projection. Other goals of this investigation are to identify other pretectal nuclear projections from the visual cortex in the guinea pig, and to determine whether there is any visuotopic organization in this pathway. Axonal tracers (biocytin or 3H-leucine) were injected into the striate cortex (Oc 1), and the tissue processed with histochemical or light autoradiographic techniques. All subcortical terminal labeling is ipsilateral in the basal ganglia and thalamic nuclei. Furthermore, projections are traced to the ipsilateral brainstem, including two areas of the pretectal complex: (1) one in the NOT, extending in some cases to the adjacent lateral portion of the posterior pretectal nucleus (PPN), and (2) one in the pars compacta of the anterior pretectal nucleus (APNc). The terminal fields in the APN are consistently located rostrally in the dorsolateral portion of the nucleus, independently of the injection site in Oc 1, whereas in the NOT the terminal fields shift slightly after injections placed in different locations in the striate cortex. A correlation of the injection sites in Oc 1 and terminal fields in the NOT reveals a loose topographic organization in the cortico-NOT projection; accordingly, the rostrocaudal axis of the striate cortex projects to the lateromedial axis of the NOT, with a 90 degrees rotation, whereas lateral parts of the striate cortex project diffusely throughout the rostrocaudal extent of the NOT. These data show for the first time that the NOT in the guinea pig receives a substantial projection from the visual cortex. Given the fact that in the guinea pig the optokinetic nystagmus shares some of the characteristics found in cat and monkey (i.e., consistent initial fast rise in the slow phase velocity and reduced asymmetry in monocular stimulation), the present findings lend support to the hypothesis that a cortical input to the NOT is a necessary condition for these oculomotor properties to be present.

E. M. Tom

Papers

Pattern of striate cortical projections to the pretectal complex in the guinea pig.