Precise olfactory responses tile the sniff cycle

Nature Neuroscience

Volumn 14, Issue 8, 2011, Pages 1039-1044

  Shusterman, Roman ^a   Smear, Matthew C ^a,b   Koulakov, Alexei A ^c   Rinberg, Dmitry ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ANIMAL EXPERIMENT; ANIMAL TISSUE; CONTROLLED STUDY; HUMAN; MALE; MITRAL CELL; NERVE CELL; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL; REVIEW; SENSORY SYSTEM; SNIFFING; TEMPORAL CORTEX;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; DISCRIMINATION (PSYCHOLOGY); MICE; MICE, INBRED C57BL; NEURONS; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; PERIODICITY; REACTION TIME; RESPIRATION; SMELL; TIME FACTORS; WAKEFULNESS;

EID: 79960834021     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2877     Document Type: Review

References (44)

1. Bair, W. & Koch, C. Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput. 8, 1185-1202 (1996). (Pubitemid 126449965)
2. Berry, M.J., Warland, D.K. & Meister, M. The structure and precision of retinal spike trains. Proc. Natl. Acad. Sci. USA 94, 5411-5416 (1997). (Pubitemid 27214797)
3. Butts, D.A. et al. Temporal precision in the neural code and the timescales of natural vision. Nature 449, 92-95 (2007). (Pubitemid 47373774)
4. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446 (2003). (Pubitemid 37490130)
5. Rieke, F., Warland, D., de Ruyter van Steveninck, R. & Bialek, W. Spikes: Exploring the Neural Code (MIT Press, Cambridge, Massachusetts, 1997).
6. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3, 884-895 (2002). (Pubitemid 135706706)
7. Chaput, M.A. Respiratory-phase-related coding of olfactory information in the olfactory-bulb of awake freely breathing rabbits. Physiol. Behav. 36, 319-324 (1986). (Pubitemid 16188277)
8. Fantana, A.L., Soucy, E.R. & Meister, M. Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59, 802-814 (2008).
9. Buonviso, N. et al. Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur. J. Neurosci. 17, 1811-1819 (2003). (Pubitemid 36645331)
10. Kepecs, A., Uchida, N. & Mainen, Z.F. The sniff as a unit of olfactory processing. Chem. Senses 31, 167-179 (2006). (Pubitemid 43231442)
11. Abraham, N.M. et al. Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44, 865-876 (2004). (Pubitemid 39575638)
12. Uchida, N. & Mainen, Z.F. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224-1229 (2003). (Pubitemid 37346044)
13. Rinberg, D., Koulakov, A. & Gelperin, A. Speed-accuracy tradeoff in olfaction. Neuron 51, 351-358 (2006). (Pubitemid 44118715)
14. Doucette, W. & Restrepo, D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 6, e258 (2008).
15. Fuentes, R.A., Aguilar, M.I., Aylwin, M.L. & Maldonado, P.E. Neuronal activity of mitral-tufted cells in awake rats during passive and active odorant stimulation. J. Neurophysiol. 100, 422-430 (2008).
16. Kay, L.M. & Laurent, G. Odor-and context-dependent modulation of mitral cell activity in behaving rats. Nat. Neurosci. 2, 1003-1009 (1999). (Pubitemid 30599564)
17. Rinberg, D., Koulakov, A. & Gelperin, A. Sparse odor coding in awake behaving mice. J. Neurosci. 26, 8857-8865 (2006). (Pubitemid 44319421)
18. Verhagen, J.V., Wesson, D.W., Netoff, T.I., White, J.A. & Wachowiak, M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10, 631-639 (2007). (Pubitemid 46652448)
19. Laurent, G., Wehr, M. & Davidowitz, H. Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837-3847 (1996). (Pubitemid 26176048)
20. Pager, J. Respiration and olfactory-bulb unit-activity in the unrestrained rat: statements and reappraisals. Behav. Brain Res. 16, 81-94 (1985). (Pubitemid 15016746)
21. Bathellier, B., Buhl, D.L., Accolla, R. & Carleton, A. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57, 586-598 (2008). (Pubitemid 351274002)
22. Bhalla, U.S. & Bower, J.M. Multiday recordings from olfactory bulb neurons in awake freely moving rats: spatially and temporally organized variability in odorant response properties. J. Comput. Neurosci. 4, 221-256 (1997). (Pubitemid 27331113)
23. Cury, K.M. & Uchida, N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585 (2010).
24. Vetter, R.S., Sage, A.E., Justus, K.A., Carde, R.T. & Galizia, C.G. Temporal integrity of an airborne odor stimulus is greatly affected by physical aspects of the odor delivery system. Chem. Senses 31, 359-369 (2006). (Pubitemid 43779037)
25. Raman, B., Joseph, J., Tang, J. & Stopfer, M. Temporally diverse firing patterns in olfactory receptor neurons underlie spatiotemporal neural codes for odors. J. Neurosci. 30, 1994-2006 (2010).
26. Nagel, K.I. & Wilson, R.I. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat. Neurosci. 14, 208-216 (2011).
27. Spors, H., Wachowiak, M., Cohen, L.B. & Friedrich, R.W. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J. Neurosci. 26, 1247-1259 (2006). (Pubitemid 43237057)
28. Shepherd, G.M. ed. The Synaptic Organization of the Brain (Oxford University Press, 2004).
29. Adrian, E.D. The electrical activity of the mammalian olfactory bulb. Electroencephalogr. Clin. Neurophysiol. 2, 377-388 (1950).
30. Sobel, E.C. & Tank, D.W. Timing of odor stimulation does not alter patterning of olfactory-bulb unit-activity in freely breathing rats. J. Neurophysiol. 69, 1331-1337 (1993). (Pubitemid 23118830)
31. 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). (Pubitemid 36175973)
32. 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). (Pubitemid 36958430)
33. Hopfield, J.J. Pattern-recognition computation using action-potential timing for stimulus representation. Nature 376, 33-36 (1995).
34. Brody, C.D. & Hopfield, J.J. Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37, 843-852 (2003). (Pubitemid 36288556)
35. Franks, K.M. & Isaacson, J.S. Strong single-fiber sensory inputs to olfactory cortex: Implications for olfactory coding. Neuron 49, 357-363 (2006). (Pubitemid 43152238)
36. Poo, C. & Isaacson, J.S. Odor representations in olfactory cortex: 'sparse' coding, global inhibition, and oscillations. Neuron 62, 850-861 (2009).
37. Haberly, L.B. & Price, J.L. Axonal projection patterns of mitral and tufted cells of olfactory-bulb in rat. Brain Res. 129, 152-157 (1977). (Pubitemid 8123259)
38. Miyamichi, K. et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191-196 (2011).
39. Stettler, D.D. & Axel, R. Representations of odor in the piriform cortex. Neuron 63, 854-864 (2009).
40. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359-365 (2002). (Pubitemid 34790758)
41. Cassenaer, S. & Laurent, G. Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448, 709-713 (2007). (Pubitemid 47236855)
42. Assisi, C., Stopfer, M., Laurent, G. & Bazhenov, M. Adaptive regulation of sparseness by feedforward inhibition. Nat. Neurosci. 10, 1176-1184 (2007). (Pubitemid 47339947)
43. Barlow, H.B. Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1, 371-394 (1972).
44. Bishop, C. Pattern Recognition and Machine Learning (Springer, 2006).