Ontogeny of cortical synaptic depression underlying olfactory sensory gating in the rat

Abstract

Sensory gating is the ability to filter irrelevant or redundant sensory input and is a critical function of all sensory systems that allows efficient processing of important stimuli. The present results demonstrate that a form of activity-dependent synaptic depression recently found to be involved in both cortical and behavioral olfactory sensory gating, is functional by at least the first postnatal week in the rat piriform cortex, and shares a common metabotropic glutamate receptor mechanism. KeywordsMetabotropic glutamate receptor; Piriform cortex; Synaptic depression; Sensory gating; Autism Sensory gating is the ability to filter irrelevant or redundant sensory input and is a critical function of all sensory systems that allows efficient processing of important stimuli. Sensory gating abnormalities have been described in several clinical disorders including autism and autism spectrum disorder [9,12,13], Fragile X syndrome [8], and schizophrenia [11]. Acute disruption of sensory gating could lead to reduced habituation, repetitive behaviors or thoughts, or general cognitive decline. However, tonic disruption of sensory gating, especially during early development, could produce more dramatic effects on both neural architecture and local circuit function. For example, given the importance of synaptic competition in shaping cortical circuit structure and function [14], a disruption of adaptation and sensory gating early in development could lead to abnormal dendritic pruning and/or cell survival.Our recent work in rats suggests that intense activation of mitral/tufted cell pre-synaptic terminals in the piriform cortex induces two forms of synaptic depression that may contribute to olfactory cortical sensory gating. One very rapidly recovering (<20 s) depression appears to be mediated by transmitter depletion, while a second intermediate duration (<2 min) depression is mediated by pre-synaptic group III metabotropic glutamate receptors (mGluR). The mGluR-mediated mechanism underlies both piriform cortical and behavioral short-term adaptation (sensory gating) to odors. Specifically, the infusion of the group II/III mGluR antagonist (RS)-α-Cyclopropyl-4-phosphonophenylglycine (CPPG) into the anterior piriform cortex (aPCX) blocks both cortical and behavioral odor adaptation, without disrupting normal odor responses [2,3]. CPPG antagonizes pre-synaptic group III mGluRs on mitral/tufted cell axons projecting to the piriform cortex and blocks activity-dependent intermediate duration synaptic depression at this synapse.In our efforts to develop a model of developmental sensory gating disorders, the present experiments served two purposes. First, although behavioral odor habituation is expressed to a similar extent and time course throughout development [6,7], we wanted to confirm that the . In all procedures described below, a concentric bipolar stainless steel stimulating electrode was placed on the lateral olfactory tract (LOT) and field potentials were recorded from layer I of the aPCX using tungsten microele...

Neurobiology of a Simple Memory

“…In vitro, electrical stimulation of mitral cell axons in a pattern mimicking mitral cell odor-evoked activity produces a similar synaptic depression (Best and Wilson 2004;Thompson et al 2005). This depression is homosynaptic (Best and Wilson 2004), perhaps contributing to the odor specificity of cortical adaptation.…”

Neurobehavioral consequences of cortical adaptation disruption during ontogeny

“…Blockade of these receptors with the antagonist (RS)-a-Cyclopropyl-4-phosphonophenylglycine (CPPG) [5] or (RS)-a-Methylserine-O-phosphate (MSOP: Kahohisa & Wilson, unpublished) prevents synaptic depression in vitro , and acute infusion of CPPG into the in vivo anterior piriform cortex prevents cortical adaptation to odors [5], habituation of odor-evoked autonomic reflexes [3], and reduces habituation of odor investigation in adult rats [30]. Furthermore, the mGluRIII-mediated synaptic depression can be expressed by at least the first postnatal week in rats [25], suggesting this mechanism is functional very early in development, as is habituation of some odorevoked autonomic reflexes [9]. …”