Roles of periventricular neurons in retinotectal transmission in the optic tectum
Introduction
In the complex natural world, the distribution and location of resources and hazards are difficult to predict for larger spaces and longer spans of time. Thus, organisms have developed senses to detect and deal with resources and hazards, evaluate and store these inputs, and generate adaptive behavior. Vision is one of the most important senses for knowing the environment, particularly to discriminate objects and detect locations.
Ablation of cortical or tectal visual areas of the brain in golden hamsters caused different types of relative blindness. Cutting of afferent and efferent fibers of the superior colliculus abolishes the ability of an individual to orient toward an object, but not the ability to identify it, according to tests of pattern discrimination learning (Schneider, 1969). Ablation of visual cortical areas has reciprocally opposite effects. Such results, obtainable only by varying the required responses as well as the stimuli in tests of visually guided behavior, might indicate a dissociation between mechanisms for two types of visuomotor control that are maintained throughout vertebrate evolution, although the possibility that the hamster is a particularly simple model system should be kept in mind. One mechanism controls the specific identification of objects, with actions directed toward or away from them. The other mechanism is concerned with the location of objects, at least insofar as controlling orientation of the head and body toward a stimulus.
These two visual pathways are referred to as the “geniculate system” and “extrageniculate system,” and they are common in all vertebrates (avian: Karten and Hodos, 1970; reptile: Hall and Ebner, 1970a, Hall and Ebner, 1970b; amphibian: Riss and Jakway, 1970, Ingle, 1973, Northcutt and Kicliter, 1980; teleost: Ito et al., 1980, Ito and Vanegas, 1983, Ito and Vanegas, 1984; cartilaginous: Ebbesson, 1972, Luiten, 1981a, Luiten, 1981b). In fish, the major retinal fibers project to the optic tectum and the extrageniculate system is well developed, due to the lack of the cortex. Thus, fish is the best animal model for studying the function of the extrageniculate system, particularly the optic tectum at the center of the system.
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Salmonid brain and tectal structure
In trout, the brain has a teleostean appearance common among the majority of other species of the same group, and the only sensory or motor specialization in trout is a visual one that results in a relatively large tectum (Meek and Nieuwenhuys, 1998). The typical features of these teleost brains are a large rhombencephalon, a large single cerebellum, two pronounced tectal halves located dorsal to the midbrain tegmentum and diencephalons, a large paired hypothalamic inferior lobe that appears as
Retinal inputs and retinorecipient cells
Retinal afferents terminate at the SO and SFGS among the six layers (Salmo: Pinganaud and Clairambault, 1979; Oncorhynchus: Shiga et al., 1989). Thus, we monitored the two-dimensional propagation of postsynaptic depolarization evoked by electrical stimulation of retinotectal afferents in the SO and SFGS using a voltage-sensitive dye and a photodiode array system to map the functional synaptic organization over a wide area of the optic tectum (Kinoshita et al., 2002). The optical recording
Functions of the extrageniculate system and memory
In mammals, ionotropic glutamate receptors are essential for long-term potentiation (LTP), which is thought of as a foundation of memory (Bliss and Collingridge, 1993). Thus, plasticity in the retinotectal synapses of rainbow trout was examined based on glutamatergic transmission using extracellular recordings of tectal slices (Kinoshita et al., 2004). Field-excitatory postsynaptic potentials (fEPSPs) were evoked by electrical stimulation of retinal fibers in the SO and SFGS. The fEPSPs were
Neuromodulatory effects of GnRH
Gonadotropin-releasing hormone (GnRH) is a decapeptide that regulates the synthesis and release of two gonadtropins (GTHs), follicle-stimulating hormone and luteinizing hormone; it thereby serves as a principal neuroendocrine mediator of reproductive function in a wide range of vertebrates (Vickers et al., 2004). It is now evident that there are two or three GnRH forms in a single vertebrate species (Oka, 2002, Yamamoto, 2003). One form of GnRH, the so-called hypothalamic GnRH, regulates
Periventricular neuron cell types
Periventricular neurons stained using biocytin-filled patch pipettes were divided into at least two types based on their dendritic morphologies. The first was a dominant group (66 out of 85 stained cells) that projected their dendrites at the most superficial layer, the SM (Fig. 3A and B). Periventricular neurons with this morphology have not been reported previously in teleosts. Many other dendrites also stem from proximal dendrites in the SFGS and SGC. An axonal branch arose from the
Isthmotectal circuit and trigger of behavior
The NI, referred to as the “parabigeminal” nucleus in mammals, lies rostrally at the level of the tegmentum proper. The nucleus is connected reciprocally and topographically with the optic tectum in amniotes, fish, and amphibians (Gruberg and Udin, 1978, Sakamoto et al., 1981, Ito et al., 1982b, Wang et al., 1983, Li et al., 1987, Tóth et al., 1994, Wiggers, 1998, Wang, 2003). In mammals, the parabigeminal nucleus also projects to a major visual nucleus in the dorsal thalamus, the dorsal
Conclusions
In the present study, periventricular neurons were identified as retinorecipient cells in the optic tectum of rainbow trout. Moreover, glutamatergic transmission between these neurons and retinal fibers were characterized as basic for tectal functions. Retinotectal transmission was potentiated in an activity-dependent manner that requires activation of NMDA receptor. In addition, retinotectal transmission was enhanced by GnRH, which is considered to be an initiator of both gonadal maturation
Acknowledgements
This study was supported by a Grant-in-Aid for Research Fellowship for Young Scientists (No. 09105) from the Japan Society for the Promotion of Science to MK, and a Grant-in-Aid (No. 16370033) from the Japan Society for the Promotion of Science and a grant from the Akiyama Foundation to EI.
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Present address: Department of Physiology, Tokyo Medical and Dental University, Graduate School and Faculty of Medicine, Tokyo 113-8519, Japan.