ABSTRACT
In mammalian olfaction, inhalation drives the temporal patterning of neural activity that underlies early olfactory processing. It remains poorly understood how the neural circuits that process incoming olfactory information are engaged in the context of inhalation-linked dynamics. Here, we used artificial inhalation and two-photon calcium imaging to compare the dynamics of activity evoked by odorant inhalation across major cell types of the mouse olfactory bulb (OB). We expressed GCaMP6f or jRGECO1a in mitral and tufted cell subpopulations, olfactory sensory neurons, and two major juxtaglomerular interneuron classes, and imaged responses to a single inhalation of odorant. Activity in all cell types was strongly linked to inhalation, and all cell types showed some variance in the latency, rise-times, and durations of their inhalation-linked response. Juxtaglomerular interneuron dynamics closely matched that of sensory inputs, while mitral and tufted cells showed the highest diversity in responses, with a range of latencies and durations that could not be accounted for by heterogeneity in sensory input dynamics. Diversity was apparent even among 'sister' tufted cells innervating the same glomerulus. Surprisingly, inhalation-linked responses of mitral and tufted cells were highly overlapping and could not be distinguished on the basis of their inhalation-linked dynamics, with the exception of a subpopulation of superficial tufted cells expressing cholecystokinin. Our results are consistent with a model in which diversity in inhalation-linked patterning of OB output arises first at the level of sensory input and is enhanced by feedforward inhibition from juxtaglomerular interneurons which differentially impact different subpopulations of OB output neurons.
SIGNIFICANCE STATEMENT Inhalation drives the temporal patterning of neural activity that underlies olfactory processing and rapid odor perception, yet the dynamics of the neural circuit elements mediating this processing are poorly understood. By comparing inhalation-linked dynamics of major olfactory bulb subpopulations, we find that diversity in the timing of neural activation arises at the level of sensory input, which is then mirrored by inhibitory interneurons in the glomerular layer. Temporal diversity is higher among olfactory bulb output neurons, with different subpopulations showing distinct but nonetheless highly overlapping ranges of inhalation-linked dynamics. These results implicate feedforward inhibition by glomerular-layer interneurons in diversifying temporal responses among output neurons, which may be important for generating and shaping timing-based odor representations during natural odor sampling.
Footnotes
Authors report no conflict of interest.
This work was supported by the National Institute on Deafness and Other Communication Disorders [F32DC016531 to S.M.S, R01DC006441 to M.W.].
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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