Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage
Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved July 9, 2013 (received for review March 6, 2013)
Significance
Even when presented with steady stimuli, sensory systems respond dynamically, including adaptation or responses after the stimuli are gone (afterimages). To measure these dynamics in smell, we recorded electrical signals from the mouse brain. We found that the neuronal representation of odors changes between breaths, and not by simple adaptation, showing that the olfactory system also undergoes these dynamics. After the end of the odor, the brain continued responding, showing that there are olfactory afterimages. Finally, we tried to isolate where afterimages are generated and found that, while the nose has some contribution, afterimages are mainly maintained in the brain.
Abstract
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.
Acknowledgments
We are grateful to Anthony Holtmaat for providing Thy1-ChR2 mice and to Richard Benton for technical assistance with the miniPID. We thank Ian Davison, Ivan Rodriguez, and members of the A.C. laboratory for helpful discussions and comments on the manuscript. This work was supported by the University of Geneva, the Swiss National Science Foundation (SNF Professor Grants PP0033_119169 and PP00P3_139189), the European Research Council (Contract ERC-2009-StG-243344-NEUROCHEMS), the National Center of Competence in Research project “SYNAPSY: The Synaptic Bases of Mental Diseases” financed by the Swiss National Science Foundation (51AU40_125759), the Novartis Foundation for Medical Research, the Carlos and Elsie de Reuter Foundation, the Ernst and Lucie Schmidheiny Foundation, and the European Molecular Biology Organization (Young Investigator Program).
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References
1
B Krekelberg, GM Boynton, RJ van Wezel, Adaptation: From single cells to BOLD signals. Trends Neurosci 29, 250–256 (2006).
2
RI Wilson, ZF Mainen, Early events in olfactory processing. Annu Rev Neurosci 29, 163–201 (2006).
3
G Mather, A Pavan, G Campana, C Casco, The motion aftereffect reloaded. Trends Cogn Sci 12, 481–487 (2008).
4
E Zwicker, “Negative afterimage” in hearing. J Acoust Soc Am 36, 2413 (1964).
5
ES Hoke, M Hoke, B Ross, Neurophysiological correlate of the auditory after-image (“Zwicker tone”). Audiol Neurootol 1, 161–174 (1996).
6
IM Vogels, AM Kappers, JJ Koenderink, Haptic aftereffect of curved surfaces. Perception 25, 109–119 (1996).
7
L Petreanu, et al., Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489, 299–303 (2012).
8
GA James, X Li, GE DuBois, L Zhou, XP Hu, Prolonged insula activation during perception of aftertaste. Neuroreport 20, 245–250 (2009).
9
SS Schiffman, DA Reilly, TB Clark, Qualitative differences among sweeteners. Physiol Behav 23, 1–9 (1979).
10
O Mazor, G Laurent, Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661–673 (2005).
11
SL Brown, J Joseph, M Stopfer, Encoding a temporally structured stimulus with a temporally structured neural representation. Nat Neurosci 8, 1568–1576 (2005).
12
H Matsumoto, H Kashiwadani, H Nagao, A Aiba, K Mori, Odor-induced persistent discharge of mitral cells in the mouse olfactory bulb. J Neurophysiol 101, 1890–1900 (2009).
13
JV Verhagen, DW Wesson, TI Netoff, JA White, M Wachowiak, Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10, 631–639 (2007).
14
J-P Rospars, P Lansky, M Chaput, P Duchamp-Viret, Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. J Neurosci 28, 2659–2666 (2008).
15
H Spors, A Grinvald, Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34, 301–315 (2002).
16
KM Cury, N Uchida, Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570–585 (2010).
17
R Shusterman, MC Smear, AA Koulakov, D Rinberg, Precise olfactory responses tile the sniff cycle. Nat Neurosci 14, 1039–1044 (2011).
18
O Gschwend, J Beroud, A Carleton, Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS ONE 7, e30155 (2012).
19
D Rinberg, A Koulakov, A Gelperin, Speed-accuracy tradeoff in olfaction. Neuron 51, 351–358 (2006).
20
NM Abraham, et al., Maintaining accuracy at the expense of speed: Stimulus similarity defines odor discrimination time in mice. Neuron 44, 865–876 (2004).
21
N Uchida, ZF Mainen, Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6, 1224–1229 (2003).
22
K Miura, ZF Mainen, N Uchida, Odor representations in olfactory cortex: Distributed rate coding and decorrelated population activity. Neuron 74, 1087–1098 (2012).
23
C Poo, JS Isaacson, Odor representations in olfactory cortex: “Sparse” coding, global inhibition, and oscillations. Neuron 62, 850–861 (2009).
24
M Kadohisa, DA Wilson, Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol 95, 1888–1896 (2006).
25
AR Best, DA Wilson, Coordinate synaptic mechanisms contributing to olfactory cortical adaptation. J Neurosci 24, 652–660 (2004).
26
BM Slotnick, JE Ptak, Olfactory intensity-difference thresholds in rats and humans. Physiol Behav 19, 795–802 (1977).
27
M Stopfer, V Jayaraman, G Laurent, Intensity versus identity coding in an olfactory system. Neuron 39, 991–1004 (2003).
28
R Vincis, O Gschwend, K Bhaukaurally, J Beroud, A Carleton, Dense representation of natural odorants in the mouse olfactory bulb. Nat Neurosci 15, 537–539 (2012).
29
M Meredith, Patterned response to odor in mammalian olfactory bulb: The influence of intensity. J Neurophysiol 56, 572–597 (1986).
30
A Rezec, B Krekelberg, KR Dobkins, Attention enhances adaptability: Evidence from motion adaptation experiments. Vision Res 44, 3035–3044 (2004).
31
A Chaudhuri, Modulation of the motion aftereffect by selective attention. Nature 344, 60–62 (1990).
32
HK Kato, MW Chu, JS Isaacson, T Komiyama, Dynamic sensory representations in the olfactory bulb: Modulation by wakefulness and experience. Neuron 76, 962–975 (2012).
33
B Bathellier, DL Buhl, R Accolla, A Carleton, Dynamic ensemble odor coding in the mammalian olfactory bulb: Sensory information at different timescales. Neuron 57, 586–598 (2008).
34
Rojas-Líbano D, Kay LM (2012) Interplay between sniffing and odorant sorptive properties in the rat. J Neurosci 32:15577–15589.
35
T Cenier, JP McGann, Y Tsuno, JV Verhagen, M Wachowiak, Testing the sorption hypothesis in olfaction: A limited role for sniff strength in shaping primary odor representations during behavior. J Neurosci 33, 79–92 (2013).
36
Gautam SH, Verhagen J V (2012) Retronasal odor representations in the dorsal olfactory bulb of rats. J Neurosci 32:7949–7959.
37
BD Philpot, TC Foster, PC Brunjes, Mitral/tufted cell activity is attenuated and becomes uncoupled from respiration following naris closure. J Neurobiol 33, 374–386 (1997).
38
S Kikuta, H Kashiwadani, K Mori, Compensatory rapid switching of binasal inputs in the olfactory cortex. J Neurosci 28, 11989–11997 (2008).
39
KR Neville, LB Haberly, Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90, 3921–3930 (2003).
40
LM Kay, et al., Olfactory oscillations: The what, how and what for. Trends Neurosci 32, 207–214 (2009).
41
AM Boyd, JF Sturgill, C Poo, JS Isaacson, Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161–1174 (2012).
42
BR Arenkiel, et al., In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205–218 (2007).
43
G Laurent, M Wehr, H Davidowitz, Temporal representations of odors in an olfactory network. J Neurosci 16, 3837–3847 (1996).
44
RW Friedrich, G Laurent, Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291, 889–894 (2001).
45
MA Chaput, H Panhuber, Effects of long duration odor exposure on the unit activity of olfactory bulb cells in awake rabbits. Brain Res 250, 41–52 (1982).
46
SA Kreher, JY Kwon, JR Carlson, The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445–456 (2005).
47
SA Montague, D Mathew, JR Carlson, Similar odorants elicit different behavioral and physiological responses, some supersustained. J Neurosci 31, 7891–7899 (2011).
48
NE Schoppa, NN Urban, Dendritic processing within olfactory bulb circuits. Trends Neurosci 26, 501–506 (2003).
49
JS Isaacson, Odor representations in mammalian cortical circuits. Curr Opin Neurobiol 20, 328–331 (2010).
50
BW Strowbridge, Role of cortical feedback in regulating inhibitory microcircuits. Ann N Y Acad Sci 1170, 270–274 (2009).
51
Y Gao, BW Strowbridge, Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb. Nat Neurosci 12, 731–733 (2009).
52
F Markopoulos, D Rokni, DH Gire, VN Murthy, Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76, 1175–1188 (2012).
53
I Fukunaga, M Berning, M Kollo, A Schmaltz, ATT Schaefer, Two distinct channels of olfactory bulb output. Neuron 75, 320–329 (2012).
54
KM Igarashi, et al., Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J Neurosci 32, 7970–7985 (2012).
55
P Dalton, Psychophysical and behavioral characteristics of olfactory adaptation. Chem Senses 25, 487–492 (2000).
56
JA Gottfried, Central mechanisms of odour object perception. Nat Rev Neurosci 11, 628–641 (2010).
57
JS Kauer, Response patterns of amphibian olfactory bulb neurones to odour stimulation. J Physiol 243, 695–715 (1974).
58
SL Turner, et al., Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474, 87–91 (2011).
59
S Charpak, J Mertz, E Beaurepaire, L Moreaux, K Delaney, Odor-evoked calcium signals in dendrites of rat mitral cells. Proc Natl Acad Sci USA 98, 1230–1234 (2001).
60
A Kohn, Visual adaptation: Physiology, mechanisms, and functional benefits. J Neurophysiol 97, 3155–3164 (2007).
61
Huk AC, Ress D, Heeger DJ (2001) Neuronal basis of the motion aftereffect reconsidered. Neuron 32(1):161–72.
62
RF Galán, M Weidert, R Menzel, AV Herz, CG Galizia, Sensory memory for odors is encoded in spontaneous correlated activity between olfactory glomeruli. Neural Comput 18, 10–25 (2006).
63
HA Zariwala, et al., A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J Neurosci 32, 3131–3141 (2012).
64
J Li, T Ishii, P Feinstein, P Mombaerts, Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428, 393–399 (2004).
65
B Bathellier, D Van De Ville, T Blu, M Unser, A Carleton, Wavelet-based multi-resolution statistics for optical imaging signals: Application to automated detection of odour activated glomeruli in the mouse olfactory bulb. Neuroimage 34, 1020–1035 (2007).
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Cover image: Francis G. Woodhouse and Raymond E. Goldstein developed and tested a computational model for the natural emergence of cytoplasmic streaming—the large-scale, active circulation of a cell's fluid contents—in plant cells through microfilament self-organization during cell development. The model, according to the authors, helps explain the patterns of cellular streaming, including pathologies seen in several species. The image is color-coded according to whether the vertical component of the vectorial order of microfilaments is positive (purple) or negative (green), and superimposed arrows show the direction of the induced cytoplasmic flow (from thin to thick). See the article by Woodhouse and Goldstein on pages 14132–14137. Image courtesy of Francis G. Woodhouse and Raymond E. Goldstein.
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Published online: August 5, 2013
Published in issue: August 27, 2013
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Acknowledgments
We are grateful to Anthony Holtmaat for providing Thy1-ChR2 mice and to Richard Benton for technical assistance with the miniPID. We thank Ian Davison, Ivan Rodriguez, and members of the A.C. laboratory for helpful discussions and comments on the manuscript. This work was supported by the University of Geneva, the Swiss National Science Foundation (SNF Professor Grants PP0033_119169 and PP00P3_139189), the European Research Council (Contract ERC-2009-StG-243344-NEUROCHEMS), the National Center of Competence in Research project “SYNAPSY: The Synaptic Bases of Mental Diseases” financed by the Swiss National Science Foundation (51AU40_125759), the Novartis Foundation for Medical Research, the Carlos and Elsie de Reuter Foundation, the Ernst and Lucie Schmidheiny Foundation, and the European Molecular Biology Organization (Young Investigator Program).
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This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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