Influencing and Interpreting Visual Input: The Role of a Visual Feedback System

Abstract

Vertebrates are able to visually identify moving objects and orient toward attractive ones or escape if the objects seem threatening. When there is more than one object in the visual field, they can attend to a particular object. The optic tectum (superior colliculus in mammals) (OT/SC) has long been known to mediate such functions (Schneider, 1969;Ingle, 1973a). Less well known is that the OT/SC is strongly affected by a smaller midbrain area called nucleus isthmi (parabigeminal nucleus in mammals) (NI/PB). We discuss how NI/PB influences OT/SC function and visual behavior.Anatomically, OT/SC makes reciprocal, topographic connections with ipsilateral NI/PB. Adjacent points in OT/SC project to adjacent points in NI/PB. The return projections from NI/PB terminate in many of the same superficial layers as retinotectal fibers, and their effects on tectal processing may facilitate selection of a single stimulus from an array of potential targets. In amphibians and mammals, NI/PB also project to the contralateral OT/SC (Fig. 1). Visual behavior and the frog NIWhen presented with a single prey stimulus anywhere in its visual field, a frog will approach and attack the stimulus. When presented with two prey stimuli, they will select one of the stimuli (Ingle, 1973b;Stull and Gruberg, 1998). After ablation of the optic tectum, frogs will not respond to prey stimuli (or to looming stimuli), although they retain other visual abilities, such as perceiving stationary objects (Ingle, 1973b).Other than the retina, the greatest input to the OT in frogs comes from NI. It can be divided into two functionally discrete regions: one region makes topographic reciprocal connections with the ipsilateral OT; the other region projects topographically to the contralateral tectal lobe. Unilateral ablation of NI results in a scotoma in the contralateral monocular visual field (Gruberg et al., 1991) that is similar to unilateral ablation of the OT. Partial ablation of NI results in a smaller scotoma that always includes the posteriormost part of the monocular field. Within the scotoma, the behavioral threshold to prey stimuli is considerably increased and resembles visual neglect.NI directly influences retinotectal transmission (King and Schmidt, 1991;Dudkin and Gruberg, 2003). Frog isthmotectal fibers are cholinergic (Desan et al., 1987;Wallace et al., 1990) and terminate in retino-recipient layers of the optic tectum. Retinal ganglion cell axons express nicotinic acetylcholine (ACh) receptors (Sargent et al., 1989). There do not appear to be conventional synapses between isthmotectal fibers and retinotectal axons (Gruberg et al., 1994). Nonetheless, by selectively filling retinotectal fibers with a fluorescent calcium-sensitive dye, NI influence on retinotectal fibers can be shown. Single-shock stimulation to the optic nerve causes a brief increase in fluorescence. Singleshock stimulation to NI causes no change in fluorescence. When single-shock stimulation of NI is paired with optic nerve stimulation, there is a greater than twofold incre...

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A Cholinergic Gating Mechanism Controlled by Competitive Interactions in the Optic Tectum of the Pigeon

“…The isthmotectal circuitry is similarly organized across vertebrate classes, and several evidence exist for it playing a role in target selection and spatial attention (Sereno and Ulinski, 1987;Gruberg et al, 1991;Winkowski and Gruberg, 2002;Cui and Malpeli, 2003;Wang et al, 2004Wang et al, , 2006Gruberg et al, 2006;Maczko et al, 2006). TGCs with remarkably similar morphology and central projections also exist in the TeO of most vertebrates.…”

Connections of Anterior Thalamic Visual Centers in the Leopard Frog, <b><i>Rana pipiens</i></b>

“…The PMDT may modulate activity of the NCZ in a pattern reminiscent of the relationship between the optic tectum and nucleus isthmi [Gruberg and Udin, 1978]. This feedback loop scheme is also found in other vertebrates [Gruberg et al, 2006], e.g., in the reciprocal connections between the thalamus and the cortex in mammals [Sherman and Guillery, 2002]. It should be noted that extracellularly applied tracers such as HRP may label fibers passing through the application area but originating from a distant area.…”