Robust Odor Coding via Inhalation-Coupled Transient Activity in the Mammalian Olfactory Bulb

Cury, Kevin M.; Uchida, Naoshige

doi:10.1016/j.neuron.2010.09.040

Cited by 262 publications

(371 citation statements)

References 62 publications

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“…Odor detection and discrimination can occur within a single breath (16,(19)(20)(21), and some have hypothesized that subsequent breaths are used for finer discrimination, as a speed-accuracy tradeoff (19,20). From this view, one might hypothesize that the changes in the odor representation reflect better discriminability between odors; however, in our data, the best odor discrimination was during the first breath.…”

Section: Discussionmentioning

confidence: 67%

“…Following realignment, many cells showed clear odor responses with precise firing within the sniff cycle (16,17). Fig.…”

Section: Resultsmentioning

confidence: 97%

“…These response percentages are similar to those observed previously (25% at 0.05% dilution in ref. 16; 60% at 2% dilution in ref. 17).…”

Section: Resultsmentioning

confidence: 99%

“…Others have measured the output of ORNs, by imaging glomeruli, and found that the response is gated by each breath and that the amplitude decreases with time (13,15). The importance of breath segmentation for M/T cells has recently been shown in awake subjects, where neurons respond with precise, phasic firing patterns (16)(17)(18). However, these recordings have focused on how information is represented during the first breath, as rodents can identify odors in a single breath (19)(20)(21).…”

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confidence: 99%

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Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Patterson

Lagier

Carleton

2013

Proc. Natl. Acad. Sci. U.S.A.

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Rodents can discriminate odors in one breath, and mammalian olfaction research has thus focused on the first breath. However, sensory representations dynamically change during and after stimuli. To investigate these dynamics, we recorded spike trains from the olfactory bulb of awake, head-fixed mice and found that some mitral cells' odor representations changed following the first breath and others continued after odor cessation. Population analysis revealed that these postodor responses contained odor-and concentration-specific information-an odor afterimage. Using calcium imaging, we found that most olfactory glomerular activity was restricted to the odor presentation, implying that the afterimage is not primarily peripheral. The odor afterimage was not dependent on odorant physicochemical properties. To artificially induce aftereffects, we photostimulated mitral cells using channelrhodopsin and recorded centrally maintained persistent activity. The strength and persistence of the afterimage was dependent on the duration of both artificial and natural stimulation. In summary, we show that the odor representation evolves after the first breath and that there is a centrally maintained odor afterimage, similar to other sensory systems. These dynamics may help identify novel odorants in complex environments.multielectrode recording | network dynamics | optogenetics S ensory systems, even when presented with fixed stimuli, use dynamic neural representations that change over time. These changes range from simple potentiation or adaptation to more complex temporal patterns (1, 2). These dynamics can persist even after the cessation of stimulus, which can take the form of an off-response or prolonged aftereffect. Aftereffects have been intensely studied in vision (1, 3) and also observed in audition (4, 5), touch (6, 7), taste (here the afterimages may be due to persistent ligand binding) (8, 9), and insect olfaction (10, 11). In mammalian olfaction, the only reported aftereffect is a "persistent afterdischarge" following high concentration odors (12).Olfaction is an active process that is coordinated by breathing (2, 13). Odorants bind to odorant receptor neurons (ORNs) in the epithelium, which synapse onto mitral/tufted (M/T) cells in the olfactory bulb (OB) at precisely defined glomeruli. Direct recordings of ORNs in rats show that ORNs are excited by odors and that activity can last for seconds after odor cessation (14). Others have measured the output of ORNs, by imaging glomeruli, and found that the response is gated by each breath and that the amplitude decreases with time (13, 15). The importance of breath segmentation for M/T cells has recently been shown in awake subjects, where neurons respond with precise, phasic firing patterns (16-18). However, these recordings have focused on how information is represented during the first breath, as rodents can identify odors in a single breath (19)(20)(21). Activity in piriform cortex is also segmented by breaths, and neurons there respond sparsely (22,23), and with a...

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Section: Discussionmentioning

confidence: 67%

“…Following realignment, many cells showed clear odor responses with precise firing within the sniff cycle (16,17). Fig.…”

Section: Resultsmentioning

confidence: 97%

“…These response percentages are similar to those observed previously (25% at 0.05% dilution in ref. 16; 60% at 2% dilution in ref. 17).…”

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Patterson

Lagier

Carleton

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Response times of 70 -90 ms (mean 76 ms) are very short considering that the first odor responses in sensory areas are detected at ϳ30 ms after odor inhalation (Cury and Uchida, 2010). Further, motor delays for limb movements in mice after optogenetic stimulation of motor cortex are ϳ25 ms (Hira et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Novel Behavioral Paradigm Reveals Lower Temporal Limits on Mouse Olfactory Decisions

Resulaj

Rinberg

2015

J. Neurosci.

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Temporallimitsonperceptualdecisionssetstrictboundariesonthepossibleunderlyingneuralcomputations.Howodorinformationisencoded in the olfactory system is still poorly understood. Here, we sought to define the limit on the speed of olfactory processing. To achieve this, we trained mice to discriminate different odor concentrations in a novel behavioral setup with precise odor delivery synchronized to the sniffing cycle. Mice reported their choice by moving a horizontal treadmill with their front limbs. We found that mice reported discriminations of 75% accuracy in 70 -90 ms after odor inhalation. For a low concentration and nontrigeminal odorant, this time was 90 -140 ms, showing that mice process odor information rapidly even in the absence of trigeminal stimulation. These response times establish, after accounting for odor transduction and motor delays, that olfactory processing can take tens of milliseconds. This study puts a strong limit on the underlying neural computations and suggests that the action potentials forming the neural basis for these decisions are fired in a few tens of milliseconds.

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Anatomy and Neurobiology of the Main and Accessory Olfactory Bulbs

Ennis

Holy

2015

Handbook of Olfaction and Gustation

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Robust Odor Coding via Inhalation-Coupled Transient Activity in the Mammalian Olfactory Bulb

Cited by 262 publications

References 62 publications

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Novel Behavioral Paradigm Reveals Lower Temporal Limits on Mouse Olfactory Decisions

Anatomy and Neurobiology of the Main and Accessory Olfactory Bulbs

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