Calcium‐fluxing glutamate receptors associated with primary gustatory afferent terminals in goldfish (Carassius auratus)

Abstract

Presynaptic ionotropic glutamate receptors modulate transmission at primary afferent synapses in several glutamatergic systems. To test whether primary gustatory afferent fibers express Ca(2+)-permeable AMPA/kainate receptors, we utilized kainate-stimulated uptake of Co(2+) along with immunocytochemistry for the Ca(2+)-binding proteins (CaBPs) calbindin and calretinin to investigate the primary gustatory afferents in goldfish (Carassius auratus). In goldfish, the primary gustatory nucleus (equivalent to the gustatory portion of the nucleus of the solitary tract) includes the vagal lobe, which is a large, laminated structure protruding dorsally from the medulla. Kainate-stimulated uptake of Co(2+) (a measure of Ca(2+)-fluxing glutamate receptors) shows punctate staining distributed in the distinct laminar pattern matching the layers of termination of the primary gustatory afferent fibers. In addition, CaBP immunocytochemistry, which correlates highly with expression of Ca(2+)-permeable AMPA/kainate receptors, shows a laminar pattern of distribution similar to that found with kainate-stimulated cobalt uptake. Nearly all neurons of the vagal gustatory ganglion show Co(2+) uptake and are immunopositive for CaBPs. Transection of the vagus nerve proximal to the ganglion results in loss of such punctate Co(2+) uptake and of punctate CaBP staining as soon as 4 days postlesion. These results are consonant with the presence of Ca(2+)-fluxing glutamate receptors on the presynaptic terminals of primary gustatory terminals, providing an avenue for modulation of primary gustatory input.

Regional chemoarchitecture of the brain of lungfishes based on calbindin D‐28K and calretinin immunohistochemistry

“…It should be mentioned that neurons containing CR and CB have been primarily associated with the GABAergic phenotype, but the presence of CB and CR in cholinergic, catecholaminergic, and nitrergic subpopultions in studies of colocalization in lungfishes and amphibians (present results; Morona & González, ; Joven, Morona, Moreno, & Gonzalez, ; López et al, ) reinforces the notion that these calcium binding proteins are not related to any neurochemical type, and might be related to the presence of calcium‐fluxing receptors in the neurons rather than the particular neurotransmitter utilized (Catania et al, ; Kondo, Okabe, Sumino, & Okado, ; Ryoo, Ahn, Lee, Kang, & Jeon, ). In line with this idea, it was found that CR expression is strongly correlated with calcium‐permeable ionotropic glutamate receptors in the neurons of the sensory zone of the vagal lobe of the goldfish (Ikenaga, Huesa, & Finger, ; Huesa, Ikenaga, Böttger, & Finger, ). Therefore, the particular content of CB and CR in a given neuron is likely associated with its physiological properties and the receptors that it expresses.…”

Immunohistochemical distribution of calretinin and calbindin (D‐28k) in the brain of the cladistian Polypterus senegalus

“…However, the results presented here would be useful for future analysis of other neurochemical markers. On the other hand, the type(s) of CaBPs expressed by a neuron appear to be subtly related to their physiological characteristics, including firing patterns (Schwaller et al, 2002;Schwaller, 2009), and may also be indicative of the type of calcium-dependent ionotropic glutamate receptors present in these neurons (Ikenaga et al, 2006;Huesa et al, 2008). Although the distribution of CaBPs in the brain of vertebrate species has been extremely useful in neuroanatomy, the particular content of CaBPs in a given neuron is likely associated with its physiological properties and the receptors that it expresses.…”

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

“…These abundant and often complementary calcium-binding protein distributions suggest a requirement for calcium regulation in these auditory brainstem neurons, all of which are characterized by high rates of activity, phase-locked responses to auditory stimuli and calcium-permeable AMPA receptors (Christensen-Dalsgaard et al, 2007; Eatock et al, 1981; Otis et al, 1995; Raman and Trussell, 1995; Trussell, 1999, 2008). Colocalization of calcium-binding proteins and Ca-permeable glutamate receptors also characterizes other sensory systems, including the goldfish vagal lobe (Huesa et al, 2008; Ikenaga et al, 2006). …”