Olfactory Bulb Coding of Odors, Mixtures and Sniffs is a Linear Sum of Odor Time Profiles

Overview

Journal Nat Neurosci

Date 2015 Jan 13

PMID 25581362

Citations 32

Authors

Priyanka Gupta

Dinu F Albeanu

Upinder S Bhalla

Affiliations

Soon will be listed here.

Abstract

The olfactory system receives intermittent and fluctuating inputs arising from dispersion of odor plumes and active sampling by the animal. Previous work has suggested that the olfactory transduction machinery and excitatory-inhibitory olfactory bulb circuitry generate nonlinear population trajectories of neuronal activity that differ across odorants. Here we show that individual mitral/tufted (M/T) cells sum inputs linearly across odors and time. By decoupling odor sampling from respiration in anesthetized rats, we show that M/T cell responses to arbitrary odor waveforms and mixtures are well described by odor-specific impulse responses convolved with the odorant's temporal profile. The same impulse responses convolved with the respiratory airflow predict the classical respiration-locked firing of olfactory bulb neurons and several other reported response properties of M/T cells. These results show that the olfactory bulb linearly processes fluctuating odor inputs, thereby simplifying downstream decoding of stimulus identity and temporal dynamics.

Citing Articles

Neural Influences on Tumor Progression Within the Central Nervous System.

Lv W, Wang Y CNS Neurosci Ther. 2024; 30(10):e70097.

PMID: 39469896 PMC: 11519750. DOI: 10.1111/cns.70097.

Human olfactory perception embeds fine temporal resolution within a single sniff.

Wu Y, Chen K, Xing C, Huang M, Zhao K, Zhou W Nat Hum Behav. 2024; 8(11):2168-2178.

PMID: 39402256 DOI: 10.1038/s41562-024-01984-8.

Behavioral discrimination and olfactory bulb encoding of odor plume intermittency.

Gumaste A, Baker K, Izydorczak M, True A, Vasan G, Crimaldi J Elife. 2024; 13.

PMID: 38441541 PMC: 11001298. DOI: 10.7554/eLife.85303.

Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb.

Zavatone-Veth J, Masset P, Tong W, Zak J, Murthy V, Pehlevan C bioRxiv. 2023; .

PMID: 37961548 PMC: 10634677. DOI: 10.1101/2023.06.21.545947.

Human Olfactory Receptor Sensor for Odor Reconstitution.

Kuroda S, Nakaya-Kishi Y, Tatematsu K, Hinuma S Sensors (Basel). 2023; 23(13).

PMID: 37448013 PMC: 10346456. DOI: 10.3390/s23136164.

References

Soucy E, Albeanu D, Fantana A, Murthy V, Meister M . Precision and diversity in an odor map on the olfactory bulb. Nat Neurosci. 2009; 12(2):210-20. DOI: 10.1038/nn.2262. View

Chalansonnet M, Chaput M . Olfactory bulb output cell temporal response patterns to increasing odor concentrations in freely breathing rats. Chem Senses. 1998; 23(1):1-9. DOI: 10.1093/chemse/23.1.1. View

Niessing J, Friedrich R . Olfactory pattern classification by discrete neuronal network states. Nature. 2010; 465(7294):47-52. DOI: 10.1038/nature08961. View

McNamara A, Magidson P, Linster C . Binary mixture perception is affected by concentration of odor components. Behav Neurosci. 2007; 121(5):1132-6. DOI: 10.1037/0735-7044.121.5.1132. View

Dhawale A, Hagiwara A, Bhalla U, Murthy V, Albeanu D . Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat Neurosci. 2010; 13(11):1404-12. PMC: 3208311. DOI: 10.1038/nn.2673. View

Martelli C, Carlson J, Emonet T . Intensity invariant dynamics and odor-specific latencies in olfactory receptor neuron response. J Neurosci. 2013; 33(15):6285-97. PMC: 3678969. DOI: 10.1523/JNEUROSCI.0426-12.2013. View

Stopfer M, Jayaraman V, Laurent G . Intensity versus identity coding in an olfactory system. Neuron. 2003; 39(6):991-1004. DOI: 10.1016/j.neuron.2003.08.011. View

Rospars J, Lansky P, Duchamp-Viret P, Duchamp A . Spiking frequency versus odorant concentration in olfactory receptor neurons. Biosystems. 2001; 58(1-3):133-41. DOI: 10.1016/s0303-2647(00)00116-7. View

Vetter R, Sage A, Justus K, Carde R, Galizia C . Temporal integrity of an airborne odor stimulus is greatly affected by physical aspects of the odor delivery system. Chem Senses. 2006; 31(4):359-69. DOI: 10.1093/chemse/bjj040. View

10.

Arevian A, Kapoor V, Urban N . Activity-dependent gating of lateral inhibition in the mouse olfactory bulb. Nat Neurosci. 2007; 11(1):80-7. PMC: 2720685. DOI: 10.1038/nn2030. View

11.

Carey R, Wachowiak M . Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J Neurosci. 2011; 31(29):10615-26. PMC: 3159407. DOI: 10.1523/JNEUROSCI.1805-11.2011. View

12.

ADRIAN E . Olfactory reactions in the brain of the hedgehog. J Physiol. 1942; 100(4):459-73. PMC: 1393326. DOI: 10.1113/jphysiol.1942.sp003955. View

13.

Lin D, Shea S, Katz L . Representation of natural stimuli in the rodent main olfactory bulb. Neuron. 2006; 50(6):937-49. DOI: 10.1016/j.neuron.2006.03.021. View

14.

Laurent G, Stopfer M, Friedrich R, Rabinovich M, Volkovskii A, Abarbanel H . Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci. 2001; 24:263-97. DOI: 10.1146/annurev.neuro.24.1.263. View

15.

Kim A, Lazar A, Slutskiy Y . System identification of Drosophila olfactory sensory neurons. J Comput Neurosci. 2010; 30(1):143-61. PMC: 3736744. DOI: 10.1007/s10827-010-0265-0. View

16.

Fukunaga I, Berning M, Kollo M, Schmaltz A, Schaefer A . Two distinct channels of olfactory bulb output. Neuron. 2012; 75(2):320-9. DOI: 10.1016/j.neuron.2012.05.017. View

17.

Broome B, Jayaraman V, Laurent G . Encoding and decoding of overlapping odor sequences. Neuron. 2006; 51(4):467-82. DOI: 10.1016/j.neuron.2006.07.018. View

18.

Wilson R, Mainen Z . Early events in olfactory processing. Annu Rev Neurosci. 2006; 29:163-201. DOI: 10.1146/annurev.neuro.29.051605.112950. View

19.

Koehl M . The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem Senses. 2005; 31(2):93-105. DOI: 10.1093/chemse/bjj009. View

20.

Brown S, Joseph J, Stopfer M . Encoding a temporally structured stimulus with a temporally structured neural representation. Nat Neurosci. 2005; 8(11):1568-76. DOI: 10.1038/nn1559. View