Olfactory cortical neurons read out a relative time code in the olfactory bulb

Nature Neuroscience

Volumn 16, Issue 7, 2013, Pages 949-957

  Haddad, Rafi ^a   Lanjuin, Anne ^a   Madisen, Linda ^b   Zeng, Hongkui ^b   Murthy, Venkatesh N ^a   Uchida, Naoshige ^a  

^a HARVARD UNIVERSITY   (United States)

^b ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NEUROBIOLOGY; NONHUMAN; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY CORTICAL NEURON; OPTOGENETICS; PHYSICAL SENSITIVITY; PIRIFORM CORTEX NEURON; PRIORITY JOURNAL; PYRIFORM CORTEX; REFRACTORY PERIOD; RELATIVE TIME CODE; RESPONSE TIME; SENSORY STIMULATION; SPIKE WAVE; ACTION POTENTIAL; ANIMAL; BRAIN MAPPING; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; ODOR; OLFACTORY SYSTEM; PATCH CLAMP TECHNIQUE; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; TIME; TRANSGENIC MOUSE;

CHANNELRHODOPSIN 2, MOUSE; OLFACTORY MARKER PROTEIN; OMP PROTEIN, MOUSE; PHOTOPROTEIN; RHODOPSIN; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21; T BOX TRANSCRIPTION FACTOR TBX21;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; DISCRIMINATION (PSYCHOLOGY); LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; ODORS; OLFACTORY BULB; OLFACTORY MARKER PROTEIN; OLFACTORY PATHWAYS; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; RHODOPSIN; SMELL; T-BOX DOMAIN PROTEINS; TIME FACTORS;

EID: 84891706960     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3407     Document Type: Article

References (54)

1. Adrian, E.D. The impulses produced by sensory nerve endings: part I. J. Physiol. (Lond.) 61, 49-72 (1926).
2. Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162-166 (1996).
3. VanRullen, R., Guyonneau, R. & Thorpe, S.J. Spike times make sense. Trends Neurosci. 28, 1-4 (2005).
4. Laurent, G. A systems perspective on early olfactory coding. Science 286, 723-728 (1999).
5. Hopfield, J.J. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33-36 (1995).
6. Spors, H. & Grinvald, A. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34, 301-315 (2002).
7. Wesson, D.W., Carey, R.M., Verhagen, J.V. & Wachowiak, M. Rapid encoding and perception of novel odors in the rat. PLoS Biol. 6, e82 (2008).
8. Macrides, F. & Chorover, S.L. Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175, 84-87 (1972).
9. Cang, J. & Isaacson, J.S. In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J. Neurosci. 23, 4108-4116 (2003).
10. Margrie, T.W. & Schaefer, A.T. Theta oscillation coupled spike latencies yield computational vigor in a mammalian sensory system. J. Physiol. (Lond.) 546, 363-374 (2003).
11. Shusterman, R., Smear, M.C., Koulakov, A.A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039-1044 (2011).
12. Cury, K.M. & Uchida, N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585 (2010).
13. Blumhagen, F. et al. Neuronal filtering of multiplexed odor representations. Nature 479, 493-498 (2011).
14. Smear, M., Shusterman, R., O'Connor, R., Bozza, T. & Rinberg, D. Perception of sniff phase in mouse olfaction. Nature 479, 397-400 (2011).
15. Miura, K., Mainen, Z.F. & Uchida, N. Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity. Neuron 74, 1087-1098 (2012).
16. Kadohisa, M. & Wilson, D.A. Olfactory cortical adaptation facilitates detection of odors against background. J. Neurophysiol. 95, 1888-1896 (2006).
17. Stettler, D.D. & Axel, R. Representations of odor in the piriform cortex. Neuron 63, 854-864 (2009).
18. Luna, V.M. & Schoppa, N.E. GABAergic circuits control input-spike coupling in the piriform cortex. J. Neurosci. 28, 8851-8859 (2008).
19. Apicella, A., Yuan, Q., Scanziani, M. & Isaacson, J.S. Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. J. Neurosci. 30, 14255-14260 (2010).
20. Davison, I.G. & Ehlers, M.D. Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 70, 82-94 (2011).
21. Dhawale, A.K., Hagiwara, A., Bhalla, U.S., Murthy, V.N. & Albeanu, D.F. Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat. Neurosci. 13, 1404-1412 (2010).
22. Arenkiel, B.R. et al. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205-218 (2007).
23. Carey, R.M., Verhagen, J.V., Wesson, D.W., Pirez, N. & Wachowiak, M. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J. Neurophysiol. 101, 1073-1088 (2009).
24. Wachowiak, M. All in a sniff: olfaction as a model for active sensing. Neuron 71, 962-973 (2011).
25. Uchida, N. & Mainen, Z.F. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224-1229 (2003).
26. Davison, I.G. & Katz, L.C. Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J. Neurosci. 27, 2091-2101 (2007).
27. Nagayama, S., Takahashi, Y.K., Yoshihara, Y. & Mori, K. Mitral and tufted cells differ in the decoding manner of odor maps in the rat olfactory bulb. J. Neurophysiol. 91, 2532-2540 (2004).
28. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300 (1995).
29. Stokes, C.C. & Isaacson, J.S. From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 67, 452-465 (2010).
30. Suzuki, N. & Bekkers, J.M. Microcircuits mediating feedforward and feedback synaptic inhibition in the piriform cortex. J. Neurosci. 32, 919-931 (2012).
31. Satou, M., Mori, K., Tazawa, Y. & Takagi, S.F. Interneurons mediating fast postsynaptic inhibition in pyriform cortex of the rabbit. J. Neurophysiol. 50, 89-101 (1983).
32. Poo, C. & Isaacson, J.S. Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations. Neuron 62, 850-861 (2009).
33. Buck, L.B. The molecular architecture of odor and pheromone sensing in mammals. Cell 100, 611-618 (2000).
34. Mori, K. & Sakano, H. How is the olfactory map formed and interpreted in the Mammalian brain? Annu. Rev. Neurosci. 34, 467-499 (2011).
35. Stopfer, M., Jayaraman, V. & Laurent, G. Intensity versus identity coding in an olfactory system. Neuron 39, 991-1004 (2003).
36. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359-365 (2002).
37. Carey, R.M. & Wachowiak, M. Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J. Neurosci. 31, 10615-10626 (2011).
38. Junek, S., Kludt, E., Wolf, F. & Schild, D. Olfactory coding with patterns of response latencies. Neuron 67, 872-884 (2010).
39. Schaefer, A.T. & Margrie, T.W. Spatiotemporal representations in the olfactory system. Trends Neurosci. 30, 92-100 (2007).
40. Haberly, L.B. Summed potentials evoked in opossum prepyriform cortex. J. Neurophysiol. 36, 775-788 (1973).
41. Franks, K.M. et al. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 72, 49-56 (2011).
42. Poo, C. & Isaacson, J.S. A major role for intracortical circuits in the strength and tuning of odor-evoked excitation in olfactory cortex. Neuron 72, 41-48 (2011).
43. Hagiwara, A., Pal, S.K., Sato, T.F., Wienisch, M. & Murthy, V.N. Optophysiological analysis of associational circuits in the olfactory cortex. Front. Neural Circuits 6, 18 (2012).
44. Mouly, A.M., Litaudon, P., Chabaud, P., Ravel, N. & Gervais, R. Spatiotemporal distribution of a late synchronized activity in olfactory pathways following stimulation of the olfactory bulb in rats. Eur. J. Neurosci. 10, 1128-1135 (1998).
45. Oswald, A.M. & Urban, N.N. Interactions between behaviorally relevant rhythms and synaptic plasticity alter coding in the piriform cortex. J. Neurosci. 32, 6092-6104 (2012).
46. Suzuki, N. & Bekkers, J.M. Neural coding by two classes of principal cells in the mouse piriform cortex. J. Neurosci. 26, 11938-11947 (2006).
47. Branco, T., Clark, B.A. & Hausser, M. Dendritic discrimination of temporal input sequences in cortical neurons. Science 329, 1671-1675 (2010).
48. Bathellier, B., Margrie, T.W. & Larkum, M.E. Properties of piriform cortex pyramidal cell dendrites: implications for olfactory circuit design. J. Neurosci. 29, 12641-12652 (2009).
49. Padmanabhan, K. & Urban, N.N. Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat. Neurosci. 13, 1276-1282 (2010).
50. Angelo, K. et al. A biophysical signature of network affiliation and sensory processing in mitral cells. Nature 488, 375-378 (2012).
51. Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793-802 (2012).
52. Yang, X.W., Model, P. & Heintz, N. Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat. Biotechnol. 15, 859-865 (1997).
53. Schmitzer-Torbert, N. & Redish, A.D. Neuronal activity in the rodent dorsal striatum in sequential navigation: separation of spatial and reward responses on the multiple T task. J. Neurophysiol. 91, 2259-2272 (2004).
54. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268 (2005).