Presynaptic Inhibition of Olfactory Sensory Neurons: New Mechanisms and Potential Functions

Abstract

Presynaptic inhibition is the suppression of neurotransmitter release from a neuron by inhibitory input onto its presynaptic terminal. In the olfactory system, the primary sensory afferents from the olfactory neuroepithelium to the brain's olfactory bulb are strongly modulated by a presynaptic inhibition that has been studied extensively in brain slices and in vivo. In rodents, this inhibition is mediated by γ-amino butyric acid (GABA) and dopamine released from bulbar interneurons. The specialized GABAergic circuit is now well understood to include a specific subset of GAD65-expressing periglomerular interneurons that stimulate presynaptic GABAB receptors to reduce presynaptic calcium conductance. This inhibition is organized to permit the selective modulation of neurotransmitter release from specific populations of olfactory sensory neurons based on their odorant receptor expression, includes specialized microcircuits to create a tonically active inhibition and a separate feedback inhibition evoked by sensory input, and can be modulated by centrifugal projections from other brain regions. Olfactory nerve output can also be modulated by dopaminergic circuitry, but this literature is more difficult to interpret. Presynaptic inhibition of olfactory afferents may extend their dynamic range but could also create state-dependent or odorant-specific sensory filters on primary sensory representations. New directions exploring this circuit's role in olfactory processing are discussed.

Odor-Specific, Olfactory Marker Protein-Mediated Sparsening of Primary Olfactory Input to the Brain after Odor Exposure

“…Neurotransmitter release from OSN presynaptic terminals is strongly modulated by presynaptic inhibition arising from GABAergic and dopaminergic periglomerular circuitry (Nickell et al, 1994;Ennis et al, 2001;McGann et al, 2005;Murphy et al, 2005;McGann, 2013). This circuit includes both a population of uniglomerular, GABAergic interneurons that express glutamic acid decarboxylase-65 (GAD65) and a separate population of multiglomerular GABAergic and dopaminergic interneurons that jointly express the transmitter synthesis enzymes GAD67 and tyrosine hydroxylase .…”

Fear Learning Enhances Neural Responses to Threat-Predictive Sensory Stimuli

“…It is also insufficient time for enhanced survival of mature CS + -responsive OSNs (which typically survive for months; (20)) to disproportionately increase their numbers. The locus of plasticity may thus lie in the glomerular circuit that presynaptically modulates OSN output (21), instead of in changes in the population of OSNs.…”

Gender and age related changes in number of dopaminergic neurons in adult human olfactory bulb

“…An increased dopaminergic activity in the OB may result in a suppression of olfaction information, due to the inhibitory effect of dopamine on the transmission between the olfactory receptor cells and the mitral cells within the olfactory glomeruli (Doty and Risser, 1989;Wilson and Sullivan, 1995;Duchamp-Viret et al, 1997;Yousem et al, 1999;Huisman et al, 2004). Although the inhibition output of olfactory receptor cells by dopamine is considered well established, a recent review offers that this literature should be interpreted with caution (McGann, 2013).…”