Role of intraglomerular circuits in shaping temporally structured responses to naturalistic inhalation-driven sensory input to the olfactory bulb

Abstract

Carey RM, Sherwood WE, Shipley MT, Borisyuk A, Wachowiak M. Role of intraglomerular circuits in shaping temporally structured responses to naturalistic inhalation-driven sensory input to the olfactory bulb. J Neurophysiol 113: 3112-3129, 2015. First published February 25, 2015 doi:10.1152/jn.00394.2014.-Olfaction in mammals is a dynamic process driven by the inhalation of air through the nasal cavity. Inhalation determines the temporal structure of sensory neuron responses and shapes the neural dynamics underlying central olfactory processing. Inhalation-linked bursts of activity among olfactory bulb (OB) output neurons [mitral/tufted cells (MCs)] are temporally transformed relative to those of sensory neurons. We investigated how OB circuits shape inhalation-driven dynamics in MCs using a modeling approach that was highly constrained by experimental results. First, we constructed models of canonical OB circuits that included mono-and disynaptic feedforward excitation, recurrent inhibition and feedforward inhibition of the MC. We then used experimental data to drive inputs to the models and to tune parameters; inputs were derived from sensory neuron responses during natural odorant sampling (sniffing) in awake rats, and model output was compared with recordings of MC responses to odorants sampled with the same sniff waveforms. This approach allowed us to identify OB circuit features underlying the temporal transformation of sensory inputs into inhalation-linked patterns of MC spike output. We found that realistic input-output transformations can be achieved independently by multiple circuits, including feedforward inhibition with slow onset and decay kinetics and parallel feedforward MC excitation mediated by external tufted cells. We also found that recurrent and feedforward inhibition had differential impacts on MC firing rates and on inhalation-linked response dynamics. These results highlight the importance of investigating neural circuits in a naturalistic context and provide a framework for further explorations of signal processing by OB networks. neural modeling; sniffing; inhibition; temporal structure; glomerulus IN THE MAMMALIAN OLFACTORY system, neural representations of olfactory information are organized into temporally discrete "packets" that are tightly coupled to the respiratory cycle (Schaefer and Margrie

A computational framework for temporal sharpening of stimulus input in the olfactory system

“…However, advantages of this configuration include the elimination of transmission of small signals, thus providing the potential for a broader range of dynamic outputs from MCs following stronger incoming signals. Recent experimental evidence supports the notion that ET cells provide the majority of excitation to MCs (De Saint Jan et al 2009;Gire et al 2012;Najac et al 2011), and the studies by Carey et al (2015) provide a previously unexplored role for ET cells in temporally constraining MC excitation. These results provide evidence that feedforward excitation arising from glutamatergic ET cells may also, or perhaps independently, contribute to the temporal refinement of MC output with respect to sensory input.…”

“…Furthermore, several classes of GABAergic neurons, both within the glomerulus itself (periglomerular, PG cells) and deeper in the olfactory bulb (granule cells, GCs), provide strong inhibition to MCs. To determine the capacity in which secondary neuronal inputs to MCs may contribute to temporal transformation of the MC input-output relationship, it is crucial first to understand how intrinsic MC conductances may similarly perform such a function.The initial model implemented by Carey et al (2015) examined how MCs might behave when directly coupled to ORNs in the absence of secondary synaptic inputs (ORN-MC model). Unsurprisingly, the ORN-MC model failed to exhibit any temporal sharpening of MC output with respect to the duration of input from ORNs in the absence of conductances generated by secondary neurons (Fig.…”

“…The initial model implemented by Carey et al (2015) examined how MCs might behave when directly coupled to ORNs in the absence of secondary synaptic inputs (ORN-MC model). Unsurprisingly, the ORN-MC model failed to exhibit any temporal sharpening of MC output with respect to the duration of input from ORNs in the absence of conductances generated by secondary neurons (Fig.…”

“…In a recent publication, Carey et al (2015) explored a series of model olfactory bulb glomerulus circuit configurations with respect to sensory input and temporal refinement of MC spike output. A major goal of this study was to better understand the cellular elements and mechanisms that transform incoming sensory signals within the earliest stages of the olfactory system.…”

“…As a starting point, Carey et al (2015) designed a model that consisted solely of direct ORN input to MCs. This circuit was designed to test the ability of intrinsic MC conductances to temporally constrain MC output.…”