Synaptic Organization and Neurotransmitters in the Rat Accessory Olfactory Bulb

Abstract

The accessory olfactory bulb (AOB) is the first relay station in the vomeronasal system and may play a critical role in processing pheromone signals. The AOB shows similar but less distinct lamination compared with the main olfactory bulb (MOB). In this study, synaptic organization of the AOB was analyzed in slice preparations from adult rats by using both field potential and patch-clamp recordings. Stimulation of the vomeronasal nerve (VN) evoked field potentials that showed characteristic patterns in different layers of the AOB. Current source density (CSD) analysis of the field potentials revealed spatiotemporally separated loci of inward current (sinks) that represented sequential activation of different neuronal components: VN activity (period I), synaptic excitation of mitral cell apical dendrites (period II), and activation of granule cells by mitral cell basal dendrites (period III). Stimulation of the lateral olfactory tract also evoked field potentials in the AOB, which indicated antidromic activation of the mitral cells (period I and II) followed by activation of granule cells (period III). Whole cell patch recordings from mitral and granule cells of the AOB supported that mitral cells are excited by VN terminals and subsequently activate granule cells through dendrodendritic synapses. Both CSD analysis and patch recordings provided evidence that glutamate is the neurotransmitter at the vomeronasal receptor neuron; mitral cell synapses and both NMDA and non-NMDA receptors are involved. We also demonstrated electrophysiologically that reciprocal interaction between mitral and granule cells in the AOB is through the dendrodendritic reciprocal synapses. The neurotransmitter at the mitral-to-granule synapses is glutamate and at the granule-to-mitral synapse is gamma-aminobutyric acid. The synaptic interactions among receptor cell terminals, mitral cells, and granule cells in the AOB are therefore similar to those in the MOB, suggesting that processing of chemosensory information in the AOB shares similarities with that in the MOB.

α2-Adrenergic receptor activation promotes long-term potentiation at excitatory synapses in the mouse accessory olfactory bulb

“…In the present experiments, field potentials were recorded from the EPL containing the reciprocal dendrodendritic synapses. The stimulation of the LOT in the mouse slice preparation evoked two sequential deflections, as originally reported in rats by Jia et al (1999) (Fig. 1A,B).…”

“…Immediately after the stimulus artifact, there was a brief negativity (N 1 ), which represents antidromic activation of the MCs. This was followed by a slower negative deflection (N 2 ), which represents a field excitatory postsynaptic potential (fEPSP) evoked in GC peripheral dendrites in the EPL, as the corresponding potential has been closely correlated with the intracellularly recorded EPSP (Jia et al 1999). The synaptic response was little affected by the NMDA receptor antagonist DL-2-amino-5-phosphonopentanoic acid (AP5), but was completely blocked by the non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX).…”

“…Synaptic connections in the external plexiform layer (EPL) of the AOB are dominated by the reciprocal dendrodendritic synapses between MCs, a single class of projection neurons, and granule cell (GC) interneurons. Glutamate released from MC dendrites activates the GC dendrites, which in turn mediate the GABAergic dendrodendritic inhibition (DDI) of the MC dendrites (Jia et al 1999;Taniguchi and Kaba 2001). This feedback inhibition at the reciprocal synapses regulates MC output (Jia et al 1999;Taniguchi and Kaba 2001;Castro et al 2007;Taniguchi et al 2013).…”

Muscarinic receptor type 1 (M1) stimulation, probably through KCNQ/Kv7 channel closure, increases spontaneous GABA release at the dendrodendritic synapse in the mouse accessory olfactory bulb

“…Along the length of the dendrites, numerous dendrodendritic reciprocal synapses are made with the dendrites of interneurones (granule cells). Glutamate is released from the mitral cell, while GABA is released from the granule cell (Jia et al, 1999;Taniguchi and Kaba, 2001). Spontaneous release of GABA from granule cells can be recorded as chloride currents in mitral cells using whole-cell recording; neuromodulators can increase the spontaneous mIPSC frequency via stimulation of noradrenergic !1 receptors (Araneda and Firestein, 2006) or mGluR1 metabotropic glutamate receptors (Castro et al, 2007).…”

Adrenergic Enhancement of Inhibitory Transmission in the Accessory Olfactory Bulb

“…First characterized in the MOB (Rall et al, 1966;Nicoll, 1969), this synapse consists of excitatory glutamatergic input from M/TCs to granule cells, which induces the release of GABA from the dendrites of granule cells, in turn inhibiting M/TCs (Isaacson and Strowbridge, 1998;Schoppa et al, 1998). This synapse has been investigated thoroughly in the MOB (Schoppa and Urban, 2003), but it has received less attention in the AOB in which it is presumed to serve a similar essential role in the processing of olfactory information (Hayashi et al, 1993;Jia et al, 1999;Taniguchi and Kaba, 2001). …”