Cholinergic innervation of the optic tectum in the frogRana pipiens

Desan, Paul H.; Gruberg, Edward R.; Grewell, Kelly M.; Eckenstein, F.

doi:10.1016/0006-8993(87)91026-2

Cited by 65 publications

(56 citation statements)

References 17 publications

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“…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).…”

Section: Visual Behavior and The Frog Nimentioning

confidence: 99%

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

et al. 2006

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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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Section: Visual Behavior and The Frog Nimentioning

confidence: 99%

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

et al. 2006

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“…Although the nucleus isthmi supplies the tectum with over 90% of its ACh (Ricciuti and Gruberg, 1985), that ACh is provided by cholinergic projections from both the ipsilateral and contralateral isthmi. These projections have differing distributions in the superficial tectal lamina making it possible that different responses arise from the activation of each of these pathways (Desan et al, 1987;Udin et al, 1990;Gruberg et al, 1994). The non-repeatability of the nicotinic receptor-evoked response versus the relative stability of the muscarinic one, also raises the possibility that sustained cholinergic input might lead to an increasingly muscarinic receptor-dominated response as nicotinic receptors desensitize.…”

Section: Understanding the Consequences Of Cholinergic Activitymentioning

confidence: 99%

“…The optic tectum of the frog provides an attractive model system for examining the ways in which cholinergic activity modulates visual system function and plasticity. Almost all of the ACh found in the amphibian tectum is supplied by a projection from the nucleus isthmi, a midbrain structure with which it is reciprocally connected (Desan et al, 1987;Marín and González, 1999). The importance of this input to system functioning is demonstrated by experiments in which the nucleus isthmi is lesioned.…”

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The effects of nicotinic and muscarinic receptor activation on patch-clamped cells in the optic tectum of rana pipiens

Debski

2003

Neuroscience

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Both nicotinic and muscarinic cholinergic receptors are present in the optic tectum. To begin to understand how the activation of these receptors affects visual activity patterns, we have determined the types of physiological responses induced by their activation. Using tectal brain slices from the leopard frog, we found that application of nicotine (100 μM) evoked long-lasting responses in 60% of patch-clamped tectal cells. Thirty percent of these responses consisted of an increase in spontaneous postsynaptic currents (sPSCs) and had both a glutamatergic and GABAergic component as determined by the use of 6-cyano-7-nitroquinoxaline-2,3-dione (50 μM) and bicuculline (25 μM), respectively. Remaining response types consisted of an inward membrane current (16%) and an increase in sPSCs combined with an inward membrane current (14%). All responses could be elicited in the presence of tetrodotoxin (0.5 μM). Muscarinic receptor-mediated responses, induced by carbachol (100 μM) application after nicotinic receptor desensitization, produced responses in 70% of tectal cells. In contrast to responses elicited by nicotine, carbachol-induced responses could be evoked multiple times without significant decrement. Responses consisted of either an outward current (57%), a decrease in sPSCs (5%) or an increase in sPSCs, with (almost 6%) or without (almost 3%) an outward current. The response elicited by carbachol was not predicted by the response of the cell to nicotine.Our results suggest that nicotinic receptors are found predominantly at presynaptic locations in the optic tectum while muscarinic receptors are most often present at postsynaptic sites. We conclude that both of these receptor types could substantially modulate visual activity by changing either the input to tectal neurons or the level of their response to that input. Keywords frog; retinotectal; acetylcholine; visual system; cholinergic; superior colliculus Acetylcholine (ACh) is present in many regions throughout the visual system appearing in the retina, superior colliculus, lateral geniculate nucleus, suprachiasmatic nuclei and the visual cortex (Groos et al., 1983;Sastry, 1985;Hohmann and Berger-Sweeney, 1998;Bickford et al., 2000). Contributed by both intrinsic and extrinsic sources (Sherman and Koch, 1986;Nobili and Sannita, 1997;Binns, 1999), cholinergic activity influences system function, plasticity and development (Greuel et al., 1988;Hohmann and Berger-Sweeney, 1998;Lauder and Schambra, 1999). Disturbances of this activity can result in such things as delayed neuronal development, changes in cytoarchitecture (Hohmann and Berger-Sweeney, 1998;Lauder and Schambra, 1999) and impaired ocular dominance shifts (Bear and Singer, 1986;Gordon et al., 1990). However, how ACh affects system activity and contributes to the mechanisms responsible for normal brain organization is not understood. The optic tectum of the frog provides an attractive model system for examining the ways in which cholinergic activity modulates visual system function and plastici...

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“…Indeed, most Ipc cells of adult pigeons have been proposed to use glycine as a neurotransmitter (Hunt et al, 1977;Streit et al, 1980;Wolfensberger et al, 1981). In addition, the presence of cholinergic neurons evidentiated with antibodies to choline acetyltransferase has been widely recognized in Ipc of fishes, amphibians, reptiles, and chickens (Brantley & Bass, 1988;Brauth et al, 1985;Desan et al, 1987;Ekstrom, 1987;Sorenson et al, 1989;Zottoli et al, 1988) as well as in Ipc of developing pigeons (Bagnoli et al, 19896 and processes reach the adult pattern around the time when the anatomical and functional maturation of the retino-tectal system is completed (Bagnoli et al, 1987). The fact that the distribution of GABAir perikarya and processes in the superficial tectal layers is modified during the early period after hatching suggests a role of incoming ganglion cell axons on the maturation of putative GABAergic systems.…”

Section: Central Visual Regionsmentioning

confidence: 99%

Changing distribution of GABA-like immunoreactivity in pigeon visual areas during the early posthatching period and effects of retinal removal on tectal GABAergic systems

et al. 1989

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The distribution of GABA-like immunoreactivity in the pigeon visual system was studied during the first 9 days after hatching using a mouse monoclonal antibody, mAb 3A12, to glutaraldehyde linked GABA . GABA-like immunoreactivity was seen in cell bodies as well as in neuropil at the level of both the retina and central visual regions at any posthatching age. However, the distribution of putative GABAergic cells and processes varied with age reaching the adult pattern at around 9 days. As a general observation, almost no cell bodies in the retina (except for some perikarya in the ganglion cell layer) were labeled at hatching but densely packed immunostained processes were present in the inner plexiform layer. During the next few days, GABA-immunoreactive amacrine and horizontal cells appeared and the adult distribution of GABA-like immunoreactivity was reached at around 9 days. In the other visual regions examined, the general trend in the variation of GABA-like immunoreactivity included: (1) a progressive decrease in the density of immunostained cell bodies and (2) an almost parallel increase in the concentration of stained neuropil. Since in pigeons the adult organization of visual pathways and the final distribution of putative GABAergic systems are reached at around the same age, we suggest the possibility that incoming ganglion cell axons play a role in regulating the distribution of GABA-like immunoreactivity in visual areas. This hypothesis is supported by the fact that the distribution of GABA-like immunoreactivity in the superficial layers of the optic tectum was altered following ablation of the contralateral retina immediately after hatching.

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Cholinergic innervation of the optic tectum in the frogRana pipiens

Cited by 65 publications

References 17 publications

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

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

The effects of nicotinic and muscarinic receptor activation on patch-clamped cells in the optic tectum of rana pipiens

Changing distribution of GABA-like immunoreactivity in pigeon visual areas during the early posthatching period and effects of retinal removal on tectal GABAergic systems

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