'Silent' Mitral Cells Dominate Odor Responses in the Olfactory Bulb of Awake Mice

Overview

Journal Nat Neurosci

Date 2014 Jul 28

PMID 25064849

Citations 38

Authors

Mihaly Kollo

Anja Schmaltz

Mostafa Abdelhamid

Izumi Fukunaga

Andreas T Schaefer

Affiliations

Soon will be listed here.

Abstract

How wakefulness shapes neural activity is a topic of intense discussion. In the awake olfactory bulb, high activity with weak sensory-evoked responses has been reported in mitral/tufted cells (M/TCs). Using blind whole-cell recordings, we found 33% of M/TCs to be 'silent', yet still show strong sensory responses, with weak or inhibitory responses in 'active' neurons. Thus, a previously missed M/TC subpopulation can exert powerful influence over the olfactory bulb.

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References

Balu R, Pressler R, Strowbridge B . Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci. 2007; 27(21):5621-32. PMC: 6672747. DOI: 10.1523/JNEUROSCI.4630-06.2007. View

Haider B, Hausser M, Carandini M . Inhibition dominates sensory responses in the awake cortex. Nature. 2012; 493(7430):97-100. PMC: 3537822. DOI: 10.1038/nature11665. View

Wachowiak M, Economo M, Diaz-Quesada M, Brunert D, Wesson D, White J . Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb. J Neurosci. 2013; 33(12):5285-300. PMC: 3690468. DOI: 10.1523/JNEUROSCI.4824-12.2013. View

Doucette W, Restrepo D . Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 2008; 6(10):e258. PMC: 2573932. DOI: 10.1371/journal.pbio.0060258. View

Abbott L, Varela J, Sen K, Nelson S . Synaptic depression and cortical gain control. Science. 1997; 275(5297):220-4. DOI: 10.1126/science.275.5297.221. View

Cang J, Isaacson J . In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci. 2003; 23(10):4108-16. PMC: 6741073. View

Wohrer A, Humphries M, Machens C . Population-wide distributions of neural activity during perceptual decision-making. Prog Neurobiol. 2012; 103:156-93. PMC: 5985929. DOI: 10.1016/j.pneurobio.2012.09.004. View

Davison I, Katz L . Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J Neurosci. 2007; 27(8):2091-101. PMC: 6673545. DOI: 10.1523/JNEUROSCI.3779-06.2007. View

Cury K, Uchida N . Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron. 2010; 68(3):570-85. DOI: 10.1016/j.neuron.2010.09.040. View

10.

Boegerhausen M, Suter P, Liu S . Modeling short-term synaptic depression in silicon. Neural Comput. 2003; 15(2):331-48. DOI: 10.1162/089976603762552942. View

11.

Margrie T, Brecht M, Sakmann B . In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 2002; 444(4):491-8. DOI: 10.1007/s00424-002-0831-z. View

12.

Pager J . Unit responses changing with behavioral outcome in the olfactory bulb of unrestrained rats. Brain Res. 1983; 289(1-2):87-98. DOI: 10.1016/0006-8993(83)90009-4. View

13.

Rinberg D, Koulakov A, Gelperin A . Sparse odor coding in awake behaving mice. J Neurosci. 2006; 26(34):8857-65. PMC: 6674368. DOI: 10.1523/JNEUROSCI.0884-06.2006. View

14.

Blauvelt D, Sato T, Wienisch M, Knopfel T, Murthy V . Distinct spatiotemporal activity in principal neurons of the mouse olfactory bulb in anesthetized and awake states. Front Neural Circuits. 2013; 7:46. PMC: 3610170. DOI: 10.3389/fncir.2013.00046. View

15.

Shoham S, OConnor D, Segev R . How silent is the brain: is there a "dark matter" problem in neuroscience?. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006; 192(8):777-84. DOI: 10.1007/s00359-006-0117-6. View

16.

Kay L, Laurent G . Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci. 1999; 2(11):1003-9. DOI: 10.1038/14801. View

17.

Matsumoto H, Kashiwadani H, Nagao H, Aiba A, Mori K . Odor-induced persistent discharge of mitral cells in the mouse olfactory bulb. J Neurophysiol. 2009; 101(4):1890-900. DOI: 10.1152/jn.91019.2008. View

18.

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

19.

Shusterman R, Smear M, Koulakov A, Rinberg D . Precise olfactory responses tile the sniff cycle. Nat Neurosci. 2011; 14(8):1039-44. DOI: 10.1038/nn.2877. View

20.

Gschwend O, Beroud J, Carleton A . Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS One. 2012; 7(1):e30155. PMC: 3260228. DOI: 10.1371/journal.pone.0030155. View