Perception of Odors Linked to Precise Timing in the Olfactory System

Rebello, Michelle R.; McTavish, Thomas S.; Willhite, David C.; Short, Shaina M.; Shepherd, Gordon M.; Verhagen, Justus V.

doi:10.1371/journal.pbio.1002021

Cited by 48 publications

(38 citation statements)

References 39 publications

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“…Here, we have shown that mammals can detect temporal features of odour stimuli at frequencies of up to 40 Hz. This surprisingly high frequency is consistent with recent findings that the olfactory bulb circuitry not only enables highly precise odour responses (Cury and Uchida, 2010;Shusterman et al, 2011) but also enables detection of optogenetically evoked inputs with a precision of 10-30 ms (Rebello et al, 2014;Smear et al, 2011). While behavioural and physiological responses to precisely timed odour stimuli have been observed in insects (Brown et al, 2005;Geffen et al, 2009;Nagel et al, 2015;Riffell et al, 2014;Szyszka et al, 2014;Vickers et al, 2001), in mammals the complex structure of the nasal cavity was generally thought to "wash-out" any temporal structure of the incoming odour plume ((Kepecs et al, 2006) see however (Gupta et al, 2015)).…”

supporting

confidence: 87%

Mammalian olfaction is a high temporal bandwidth sense

Erskine

Ackels

Dasgupta

et al. 2019

Preprint

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Odours are transported in turbulent plumes resulting locally in highly fluctuating odour concentration (Celani et al., 2014;Murlis et al., 1992;Mylne and Mason, 1991;Shraiman and Siggia, 2000). Yet, whether mammals can make use of the ensuing temporal structure (Celani et al., 2014;Crimaldi and Koseff, 2001;Murlis et al., 1992;Mylne and Mason, 1991;Schmuker et al., 2016;Vickers, 2000) to extract information about the olfactory environment remains unknown. Here, we use dual-energy photoionisation recording with >300 Hz bandwidth to simultaneously determine odour concentrations of two odours in air. We show that temporal correlation of odour concentrations reliably predicts whether odorants emerge from the same or different sources in normal turbulent environments outside and in laboratory conditions. To replicate natural odour dynamics in a reproducible manner we developed a multichannel odour delivery device allowing presentation of several odours with 10 ms temporal resolution. Integrating this device in an automated operant conditioning system we demonstrate that mice can reliably discriminate the correlation structure of odours at frequencies of up to 40 Hz. Consistent with this finding, output neurons in the olfactory bulb show segregated responses depending on the correlation of odour stimuli with populations of 10s of neurons sufficient to reach behavioural performance. Our work thus demonstrates that mammals can perceive temporal structure in odour stimuli at surprisingly fast timescales. This in turn might be useful for key behavioural challenges (Jacobs, 2012) such as odour source separation (Hopfield, 1991), figure-ground separation (Rokni et al., 2014) or odour localisation (Vergassola et al., 2007;Vickers, 2000). Main TextThe turbulent nature of air as well as water flow results in complex temporal fluctuations of odour concentrations that depend on the distance and direction of odour sources (Atema, 1995;Baker et al.

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supporting

confidence: 87%

Mammalian olfaction is a high temporal bandwidth sense

Erskine

Ackels

Dasgupta

et al. 2019

Preprint

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“…Both the spatial identity or temporal latencies of glomeruli activated in the pattern may be perceptually meaningful (6,7), but the relative importance of each is unknown. It is also unclear what forms a perceptually-meaningful combination of glomerular activation: ordered sequences aligned relative to each other (10)(11)(12), sequences aligned to sniff rhythm (6,7,13,14), or the earliest activated subset of glomeruli within a sniff rhythm (15,16).…”

Section: Introductionmentioning

confidence: 99%

Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception

Chong

Moroni

Wilson

et al. 2019

Preprint

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How does neural activity generate perception? The spatial identities and temporal latencies of activated units correlate with external sensory features, but finding the principal activity subspace that is consequential for perception, remains challenging. We trained mice to recognize synthetic odors constructed from parametrically-defined patterns of optogenetic activation, then measured perceptual changes during extensive and controlled perturbations across spatiotemporal dimensions. We modelled recognition as the matching of patterns to learned templates, finding that perceptually-meaningful templates are sequences of spatially-identified units, ordered by latencies relative to each other (with minimal effects of sniff). Within templates, individual units contribute additively, with larger contributions from earlier-activated units. Our synthetic approach reveals the fundamental logic of the olfactory code, and provides a general framework for testing links between sensory activity and perception.

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“…Inhalation delivers transient pulses of odorant to the olfactory epithelium, and so determines the initial temporal structure of olfactory sensory input to the brain and drives the temporal patterning of activity at subsequent processing stages (Macrides and Chorover, 1972, Onoda and Mori, 1980, Sobel and Tank, 1993, Kepecs et al, 2006, Schaefer et al, 2006, Schaefer and Margrie, 2007, Wachowiak, 2011. Behavioral and psychophysical studies have shown that odor percepts are formed within the time of a single inhalation (150-250 ms for rodents, ~400 ms for humans) (Laing, 1986, Johnson et al, 2003, Kepecs et al, 2007, and neurophysiological studies have demonstrated that the temporal pattern of neural activity elicited by a single inhalation of odorant can robustly encode odorant identity and intensity (Uchida and Mainen, 2003, Kepecs et al, 2007, Wesson et al, 2008, Cury and Uchida, 2010, Shusterman et al, 2011, Rebello et al, 2014. Thus, understanding how inhalation-linked temporal patterns of activity are generated and shaped by neural circuits in the early olfactory pathway is fundamental to understanding olfactory information processing.…”

Section: Introductionmentioning

confidence: 99%

Temporal dynamics of inhalation-linked activity across defined subpopulations of mouse olfactory bulb neurons imaged in vivo

Short

Wachowiak

2019

Preprint

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In mammalian olfaction, inhalation drives the temporal patterning of neural activity that underlies early olfactory processing, and a single inhalation of odorant is sufficient for odor perception. However, how the neural circuits that process incoming olfactory information are activated in the context of inhalation-linked dynamics remains poorly understood. To better understand early olfactory processing in vivo, we used an artificial inhalation paradigm combined with two-photon calcium imaging to compare the dynamics of activity evoked by odorant inhalation across major cell types of the mouse olfactory bulb. Transgenic models and cell-type specific genetic tools were used to express GCaMP6f or jRGECO1a in mitral and tufted cell subpopulations, olfactory sensory neurons and two major juxtaglomerular interneuron classes, and responses to a single inhalation of odorant were compared. 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 patterns. The dynamics of juxtaglomerular interneuron activity closely matched that of sensory neuron inputs, while mitral and tufted cells showed the highest diversity in dynamics, with a range of latencies and durations that could not be accounted for by heterogeneity in the dynamics of sensory input. Surprisingly, temporal response patterns of mitral and superficial tufted cells were highly overlapping such that these two subpopulations could not be distinguished on the basis of their inhalation-linked dynamics, with the exception of a subpopulation of superficial tufted cells expressing the peptide transmitter cholecystokinin. Overall, these results support a model in which diversity in inhalation-linked patterning of OB output arises first at the level of OSN inputs to the OB and is enhanced by feedforward inhibition from juxtaglomerular interneurons which differentially impacts different subpopulations of OB output neurons.

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Perception of Odors Linked to Precise Timing in the Olfactory System

Abstract: The temporal dynamics of glomeruli activity can be behaviorally discerned by mice down to 13 milliseconds.

Cited by 48 publications

References 39 publications

Mammalian olfaction is a high temporal bandwidth sense

Mammalian olfaction is a high temporal bandwidth sense

Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception

Temporal dynamics of inhalation-linked activity across defined subpopulations of mouse olfactory bulb neurons imaged in vivo

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