Why sniff fast? The relationship between sniff frequency, odor discrimination, and receptor neuron activation in the rat

Journal of Neurophysiology

Volumn 101, Issue 2, 2009, Pages 1089-1102

  Wesson, Daniel W ^a,c   Verhagen, Justus V ^a,d   Wachowiak, Matt ^a,b  

^a Boston University   (United States)

^b Boston University   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; LICKING; LOCOMOTION; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY RECEPTOR; PRIORITY JOURNAL; RAT; SMELLING; SNIFFING;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; DISCRIMINATION (PSYCHOLOGY); FEMALE; ODORS; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; PSYCHOPHYSICS; RATS; RATS, LONG-EVANS; REACTION TIME; SMELL; TIME FACTORS;

EID: 61349117402     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90981.2008     Document Type: Article

References (65)

1. Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, Schaefer AT. Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44: 865-876, 2004.
2. Ambros-Ingerson J, Granger R, Lynch G. Simulation of paleocortex performs hierarchical clustering. Science 247: 1344-1348, 1990.
3. Arevian AC, Kapoor V, Urban NN. Activity-dependent gating of lateral inhibition in the mouse olfactory bulb. Nat Neurosci 11: 80-87, 2008.
4. Bodyak N, Slotnick B. Performance of mice in an automated olfactometer: odor detection, discrimination and odor memory. Chem Senses 24: 637-645, 1999.
5. Bramble DM, Carrier DR. Running and breathing in mammals. Science 219: 251-256, 1983.
6. Budick SA, Dickinson MH. Free-flight responses of Drosophila melanogaster to attractive odors. J Exp Biol 209: 3001-3017, 2006.
7. Carvell GE, Simons DJ. Task- and subject-related differences in sensorimotor behavior during active touch. Somatosens Mot Res 12: 1-9, 1995.
8. Carey RC, Verhagen JV, Wesson DW, Pirez N, Wachowiak M. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J Neurophysiol 101: 1073-1088, 2009.
9. Castelhano MS, Henderson JM. Stable individual differences across images in human saccadic eye movements. Can J Exp Psychol 62: 1-14, 2008.
10. Catania KC, Hare JF, Campbell KL. Water shrews detect movement, shape, and smell to find prey underwater. Proc Natl Acad Sci USA 105: 571-576, 2008.
11. Clarke S. Sniffing and fixed-ratio behavior for sucrose and brain stimulation reward in the rat. Physiol Behav 7: 695-699, 1971.
12. Clarke S, Trowill JA. Sniffing and motivated behavior in the rat. Physiol Behav 6: 49-52, 1971.
13. Clevenger AC, Restrepo D. Evaluation of the validity of a maximum likelihood adaptive staircase procedure for measurement of olfactory detection threshold in mice. Chem Senses 31: 9-26, 2006.
14. Dethier VG. Sniff, flick, and pulse: an appreciation of interruption. Proc Am Philos Soc 131: 159-176, 1987.
15. Doty RL, Ferguson-Segall M, Lucki I, Kreider M. Effects of intrabulbar injections of 6-hydroxydopamine on ethyl acetate odor detection in castrate and non-castrate male rats. Brain Res 444: 95-103, 1988.
16. Freeman WJ, Viana Di Prisco G, Davis GW, Whitney TM. Conditioning of relative frequency of sniffing by rabbits to odors. J Comp Neurol 97: 12-23, 1983.
17. Goldberg SJ, Moulton DG. Olfactory bulb responses telemetered during an odor discrimination task in rats. Exp Neurol 96: 430-442, 1987.
18. Goldman JA, Patek SN. Two sniffing strategies in palinurid lobsters. J Exp Biol 205: 3891-3902, 2002.
19. Harrison JM. The control of responding by sounds: unusual effect of reinforcement. J Exp Anal Behav 32: 167-181, 1979.
20. Hayar A, Karnup S, Shipley MT, Ennis M. Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J Neurosci 24: 1190-1199, 2004.
21. Ikemoto S, Panksepp J. The relationship between self-stimulation and sniffing in rats: does a common brain system mediate these behaviors? Behav Brain Res 61: 143-162, 1994.
22. Johnson BN, Mainland JD, Sobel N. Rapid olfactory processing implicates subcortical control of an olfactomotor system. J Neurophysiol 90: 1084-1094, 2003.
23. Karpov AP. Analysis of neuron activity in the rabbit's olfactory bulb during food-acquisition behavior. In: Neural Mechanisms of Goal-Directed Behavior and Learning, edited by Thompson RF, Hicks LH, Shvyrkov VB. New York: Academic Press, 1980, p. 273-282.
24. Katz DB, Simon SA, Nicolelis MA. Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci 21: 4478-4489, 2001.
25. Kay LM. Theta oscillations and sensorimotor performance. Proc Natl Acad Sci USA 102: 3863-3868, 2005.
26. Kelliher KR, Ziesmann J, Munger SD, Reed RR, Zufall F. Importance of the CNGA4 channel gene for odor discrimination and adaptation in behaving mice. Proc Natl Acad Sci USA 100: 4299-4304, 2003.
27. Kent PF, Mozell MM, Murphy SJ, Hornung DE. The interaction of imposed and inherent olfactory mucosal activity patterns and their composite representation in a mammalian species using voltage-sensitive dyes. J Neurosci 16: 345-353, 1996.
28. Kepecs A, Uchida N, Mainen ZF. The sniff as a unit of olfactory processing. Chem Senses 31: 167-179, 2006.
29. Kepecs A, Uchida N, Mainen ZF. Rapid and precise control of sniffing during olfactory discrimination in rats. J Neurophysiol 98: 205-213, 2007.
30. Komisaruk BR. Synchrony between limbic system theta activity and rhythmical behavior in rats. J Comp Physiol Psychol 70: 482-492, 1970.
31. Laing DG. Characterization of human behaviour during odour perception. Perception 11: 221-230, 1982.
32. Macrides F. Temporal relationships between hippocampal slow waves and exploratory sniffing in hamsters. Behav Biol 14: 295-308, 1975.
33. Macrides F, Eichenbaum HB, Forbes WB. Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2: 1705-1711, 1982.
34. Mainland J, Sobel N. The sniff is part of the olfactory percept. Chem Senses 31: 181-196, 2006.
35. Mozell MM. Evidence for a chromatographic model of olfaction. J Gen Physiol 56: 46-63, 1970.
36. Mozell MM, Kent PF, Murphy SJ. The effect of flow-rate upon the magnitude of the olfactory response differs for different odorants. Chem Senses 16: 631-649, 1991.
37. Mozell MM, Sheehe PR, Hornung DE, Kent PF, Youngentob SL, Murphy SJ. Imposed and inherent mucosal activity patterns. J Gen Physiol 90: 625-650, 1987.
38. Nevitt GA. Do fish sniff? A new mechanism of olfactory sampling in pleuronectid flounders. J Exp Biol 157: 1-18, 1991.
39. Pager J. Respiration and olfactory bulb unit activity in the unrestrained rat: statements and reappraisals. Behav Brain Res 16: 81-94, 1985.
40. Porter JC, Craven B, Khan RM, Chang S, Kang I, Judkewitz B, Volpe J, Settles G, Sobel N. Mechanisms of scent-tracking in humans. Nat Neurosci 10: 27-29, 2007.
41. Rajan R, Clement JP, Bhalla US. Rats smell in stereo. Science 311: 666-670, 2006.
42. Randall DC, Brown DR. Stability of visceral behavior in the awake rat during rest. J Exp Anal Behav 61: 273-279, 1994.
43. Rinberg D, Koulakov A, Gelperin A. Speed-accuracy tradeoff in olfaction. Neuron 51: 351-358, 2006.
44. Schaefer AT, Margrie TW. Spatiotemporal representations in the olfactory system. Trends Neurosci 30: 92-100, 2007.
45. Schmitt BC, Ache BW. Olfaction: responses of a decapod crustacean are enhanced by flicking. Science 205: 204-206, 1979.
46. Schoenfeld TA, Cleland TA. The anatomical logic of smell. Trends Neurosci 28: 620-627, 2005.
47. Schoenfeld TA, Cleland TA. Anatomical contributions to odorant sampling and representation in rodents: zoning in on sniffing behavior. Chem Senses 31: 131-144, 2006.
48. Slotnick B. Olfactory performance of rats after selective deafferentation of the olfactory bulb by 3-methyl indole. Chem Senses 32: 173-181, 2007.
49. Slotnick BM, Nigroshi BJ. Olfactory stimulus control evaluated in a small animal olfactometer. Percept Mot Skills 39: 583-597, 1974.
50. Sobel N, Khan RM, Hartley CA, Sullivan EV, Gabrieli JD. Sniffing longer rather than stronger to maintain olfactory detection threshold. Chem Senses 25: 1-8, 2000.
51. Sorwell KG, Wesson DW, Baum MJ. Sexually dimorphic enhancement by estradiol of male urinary odor detection thresholds in mice. Behav Neurosci 122: 788-793, 2008.
52. Steen JB, Mohus I, Kvesetberg TK, Walloe L. Olfaction in bird dogs during hunting. Acta Physiol Scand 157: 115-119, 1996.
53. Thesen A, Steen JB, Doving KB. Behaviour of dogs during olfactory tracking. J Exp Biol 180: 247-251, 1993.
54. Uchida N, Kepecs A, Mainen ZF. Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci 7: 485-491, 2006.
55. Uchida N, Mainen ZF. Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6: 1224-1229, 2003.
56. Verhagen JV, Wesson DW, Netoff TI, White JA, Wachowiak M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10: 631-639, 2007.
57. Wachowiak M, Shipley MT. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17: 411-423, 2006.
58. Walker JKL, Lawson BL, Jennings DB. Breath timing, volume and drive to breathe in conscious rats: comparative aspects. Respir Physiol 107: 241-250, 1997.
59. Welker WI. Analysis of sniffing in the albino rat. Behavior 22: 223-244, 1964.
60. Wesson DW, Carey RM, Verhagen JV, Wachowiak M. Rapid encoding and perception of novel odors in the rat. PLoS Biol 6: e82, 2008a.
61. Wesson DW, Donahou TN, Johnson MO, Wachowiak M. Sniffing behavior of mice during performance in odor-guided tasks. Chem Senses 33: 581-596, 2008b.
62. Whishaw IQ, Tomie JA. Olfaction directs skilled forelimb reaching in the rat. Behav Brain Res 32: 11-21, 1989.
63. Young TA, Wilson DA. Frequency-dependent modulation of inhibition in the rat olfactory bulb. Neurosci Lett 276: 65-67, 1999.
64. Youngentob SL. A method for the rapid automated assessment of olfactory function. Chem Senses 30: 219-229, 2005.
65. Youngentob SL, Mozell MM, Sheehe PR, Hornung DE. A quantitative analysis of sniffing strategies in rats performing odor discrimination tasks. Physiol Behav 41: 59-69, 1987.