Colocalization of somatostatin with GABA or glutamate in distinct afferent terminals presynaptic to the Mauthner cell

Abstract

The presence of somatostatin in afferent fibers impinging on the goldfish Mauthner (M-) cell was determined using immunohistochemical methods, combined with confocal and electron microscopy, and the relationship of this peptide with inhibitory and excitatory terminals was studied. Somatostatin-reactive boutons were present only on the distal part of the M-cell's lateral dendrite. Somatostatin immunoreactivity was observed in typical large myelinated club endings (LMCEs) corresponding to mixed (electrical and chemical) eighth nerve primary afferent fibers. The axoplasm of these fibers contained dense- core vesicles (DCVs) dispersed among round vesicles. We have made a novel finding that the excitatory transmitter glutamate is present in LMCEs. Colocalization of this amino acid with somatostatin was detected in 75% of these endings using postembedding staining with gold particles of various sizes. The other structures labeled by somatostatin antibody were found to be small vesicle boutons (SVBs), which establish symmetrical synapses and contain a population of pleiomorphic vesicles with DCVs scattered among them. Double labeling with antibodies against glutamic acid decarboxylase and GABA allowed the definition of three types of biochemically characterized terminals: [somatostatin-GABA], [GABA], and [somatostatin]. However, the occurrence of DCVs in SVBs stained for GABA alone suggests that neuropeptides other than somatostatin may also coexist with GABA in this class of boutons. The coexistence of somatostatin with both inhibitory and excitatory neurotransmitters acting on the same region of a postsynaptic cell is discussed in relation to the role postulated for this peptide in synaptic plasticity.

Morphology of the release site of inhibitory synapses on the soma and dendrite of an identified neuron

“…Four compartments were defined, the axon cap (AC), the soma outside the AC (S) and the medial (mLD) and distal (dLD) parts of the lateral dendrite (150-200 and 350-450 km away from the soma, respectively). We have chosen these sectors because the distributions of glycine-and GABAcontaining boutons are well-characterized on the soma and on the lateral dendrite (Korn et al, 1990;Petrov et al, 1991;Triller et al, 1993;Sur et al, 1994).…”

Serotonergic modulation of startle-escape plasticity in an African cichlid fish: a single-cell molecular and physiological analysis of a vital neural circuit

“…In goldfish, for example, dopamine enhances the efficacy of excitatory synapses to the M-cell LD (Pereda et al 1992(Pereda et al , 1994. Also in goldfish, the neuropeptide somatostatin is colocalized with glutamatergic excitatory and GABAergic inhibitory synaptic contacts that impinge onto the M-cell, an arrangement suggesting a modulatory role for this neuropeptide (Sur et al 1994). Indeed, local application of somatostatin onto the M-cell LD increases excitatory synaptic transmission in the large club endings that provide auditory input to the cell (Pereda et al 1997).…”

Social and Ecological Regulation of a Decision-Making Circuit

“…However, our experiments cannot exclude the possibility that the larger PSPs in DOMs may be also mediated by modulating the efficacy of excitatory synaptic transmission at the mixed electrotonic and chemical junctions between the large eighth nerve endings and the M-cell (Pereda et al 1992(Pereda et al , 1994. For example, in goldfish, local application of the neuropeptide somatostatin onto the M-cell lateral dendrite increases excitatory synaptic transmission (Pereda et al 1997), and somatostatin has been shown to be co-localized with glutamatergic excitatory but also with GABAergic inhibitory synaptic contacts onto the M-cell (Sur et al 1994). These findings are interesting because somatostatin also controls social behavior in A. burtoni (Hofmann and Fernald 2000;Hofmann 2006, 2007) and thus constitutes one candidate for the proposed neuromodulatory link between social state and M-cell excitability.…”