Benchmark II agv13

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Sniffing


Sniffing is a perceptually-relevant behavior, defined as the active sampling of odors through the nasal cavity for the purpose of information acquisition. This behavior, displayed by all terrestrial vertebrates, is typically identified based upon changes in respiratory frequency and/or amplitude[1] [2] , and is often studied in the context of odor guided behaviors and olfactory perceptual tasks. Sniffing is quantified by measuring intra-nasal pressure or flow or air[3] [4] [5] [6] or, while less accurate, through a stain gauge on the chest to measure total respiratory volume[7] . Strategies for sniffing behavior vary depending upon the animal, with small animals (rats, mice, hamsters) displaying sniffing frequencies ranging from 4-12Hz[2] [3] [8] , but larger animals (humans) sniffing at much slower frequencies, usually <2Hz[7] [9] . Subserving sniffing behaviors, evidence for an ‘olfactomotor’ circuit in the brain exists[10] [11] , wherein perception or expectation of an odor can trigger brain respiratory centers to allow for the modulation of sniffing frequency and amplitude and thus acquisition of odor information. Sniffing is analogous to other stimulus sampling behaviors, including visual saccades, active touch, and whisker movements in small animals (viz., whisking)[12] [13] . Atypical sniffing has been reported in cases of neurological disorders, especially those disorders characterized by impaired motor function and olfactory perception[14] [15] .

Sniffing.

Background and history of sniffing

Background

The behavior of sniffing incorporates changes in air flow within the nose. This can involve changes in the depth of inhalation and the frequency of inhalations. Both of these entail modulations in the manner whereby air flows within the nasal cavity and through the nostrils. Consequentially, when the air being breathed is odorized, odors can enter and leave the nasal cavity with each sniff. The same applies regardless of what gas is being inhaled, including toxins and solvents, and other industrial chemicals which may be inhaled as a form of drug abuse [16] .

The act of sniffing is considered distinct from respiration along several grounds. In humans, one can assess the occurrence of a sniff based upon volitional control of air movement through the nose[17] . In these cases, human subjects can be asked to inhale for a certain amount of time, or in a particular pattern[7] . Some animals are obligate nasal breathers, wherein the only air for respiration must arrive into the lungs via the nose. This includes rats and mice. Thus, in these animals the distinction between a breath and a sniff is not clear and could be argued indistinguishable[18] . See section III., Sniffing in small animals.

Sniffing is observed among all terrestrial vertebrates, wherein they inhale environmental air[19] . Interestingly, though, sniffing may also occur in underwater environments wherein an animal may exhale air from within its lungs and nasal cavity to acquire odors within an aquatic environment and then re-inhale this air[20] . See section III., Sniffing in small animals, section b.

While sniffing behavior is often observed and discussed within the context of acquiring odor information, sniffing is also displayed during the performance of motivated behaviors and upon deep brain electrical stimulation of brain reward centers. For instance, prior to obtaining a food reward, mice and rabbits increase their sniffing frequency[3] [21] in a manner independent of seeking odor information. Sniffing behavior is also displayed by animals upon involuntary electrical stimulation of numerous brain structures[22] . Thus, while sniffing is often considered a critical part of olfaction, its link with motivated and reward behaviors suggests it plays a role in other behaviors.

History

It was thought within the medical community, starting as early as the 19th century, that air flow within the nose was essential for olfaction. An XXXXXXX physician, Dr. XXXXXXXXXXXXXXXXXXX, provided a demonstration in front of his colleagues in the year XXXX wherein he laid a human subject on his back and poured perfume into his nose. He asked the subject to report whether he smelled an odor or not, at which time the subject replied he was unable to smell anything. This reported demonstration gave early evidence that without air flow to transport odors within the nasal cavity, no percept resulted.

Studies into the perceptual correlates of sniffing on human olfaction did not reach the mainstream scientific community until the 1950s. Frank Jones, an American Psychologist, published a paper demonstrating the interplay between parameters of sniffing and odor detection thresholds. He found that deep sniffs, consisting of a large volume of air, allowed for consistent and accurate detection of odors[23] .

One of the earliest reports of exploring sniffing in non-human animals was provided by Welker in his 1964 article, Analysis of sniffing in the albino rat[1] . In this study, Welker used video recordings of rats during presentation with odors and other stimuli to explore the chest movements as an index of sniffing. This was the first paper to report that rats can sniff at frequencies reaching 12Hz upon detection of odors and during free exploration. This paper also provided early evidence that the rhythm of sniffing was coupled with other sensory behaviors, such as whisking, or the movement of the whiskers.

While behavioral and psychophysical studies into sniffing and its influence on odor perception began to surface, much less work was being performed to explore the influence of sniffing behaviors on the physiological processing of odors within the brain. Early recordings from the olfactory bulbs of hedgehogs by Lord Edgar Adrian, who previously won the 1932 Nobel Prize along with Sir Charles Scott Sherrington for their work on the functions of neurons, revealed that field potential oscillations within the hedgehog olfactory bulb were entrained to the respiratory cycle [24] . Further, odor-evoked oscillations (including an exhaled puff form a pipe), were amplified along with the respiratory cycle. These data gave evidence that information processing within the brain, particularly that of odors, was linked with respiration – establishing the integral nature of sniffing for the physiological processing of odors. About 20 years later, Max Mozell published a series of studies wherein he further proposed that the flow rate and the sorptive properties of odorants interplay to effect the location of odorant binding to olfactory receptor neurons in the nose and consequentially odor input to the brain[25] . Later, evidence that single neurons in the olfactory bulb, the brains first relay station for odor information, are entrained with respiration was presented, establishing a solid basis for the control of odor input to the brain and the processing of odors by sniffing [26] .

Methods for quantifying sniffing

Video

Chest strain

Nasal microphone

Nasal thermocouple

Nasal pressure

Sniffing in small animals

Early studies in rats

Sniffing in freely exploring rodents

Sniffing during odor guided tasks

Sniffing in semi-aquatic animals

Sniffing and control of odor input to the brain

Sniffing in humans

Sniffing versus Smelling

Functional imaging of sniff-evoked activity

Neural control of sniffing

Evidence for an olfactomotor loop

Relation of sniffing to other stimulus sampling behaviors

Whisking

Saccades

Touch

Licking

Relevance to neurological disorders

Alzheimer’s disease

Parkinson’s disease


References

[1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26]

  1. ↑ 1.0 1.1 1.2 Welker, WI (1964). "Analysis of sniffing in the albino rat". Behavior (22): 223–244. 
  2. ↑ 2.0 2.1 2.2 Youngentob, S.L.; Mozell, M. M., Sheehe, P. R. & Hornung, D. E. (1987). "A quantitative analysis of sniffing strategies in rats performing odor discrimination tasks". Physiol Behav. 41: 59–69.  Cite uses deprecated parameter |coauthors= (help)
  3. ↑ 3.0 3.1 3.2 3.3 Wesson, D. W.; Donahou, T. N., Johnson, M. O. & Wachowiak, M (2008). "Sniffing behavior of mice during performance in odor-guided tasks". Chem Senses (33): 581–596.  Cite uses deprecated parameter |coauthors= (help)
  4. ↑ 4.0 4.1 Verhagen, J. V.; Wesson, D. W., Netoff, T. I., White, J. A. & Wachowiak, M (2007). "Sniffing controls an adaptive filter of sensory input to the olfactory bulb". Nat Neurosci (10): 631–639.  Cite uses deprecated parameter |coauthors= (help)
  5. ↑ 5.0 5.1 Uchida, N; Mainen, Z. F (2003). "Speed and accuracy of olfactory discrimination in the rat". Nat Neurosci (6): 1224–1229.  Cite uses deprecated parameter |coauthors= (help)
  6. ↑ 6.0 6.1 Macrides, F; Eichenbaum, H. B. & Forbes, W. B (1982). "Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning". J Neurosci (2): 1705–1711.  Cite uses deprecated parameter |coauthors= (help)
  7. ↑ 7.0 7.1 7.2 7.3 Laing, D. G. (1983). "Natural sniffing gives optimum odour perception for humans". Perception (12): 99–117. 
  8. ↑ 8.0 8.1 Vanderwolf, C. H. (1992). "Hippocampal activity, olfaction, and sniffing: an olfactory input to the dentate gyrus". Brain Research (593): 197–208. 
  9. ↑ 9.0 9.1 Sobel, N.; Prabhakaran, J. E. Desmond, G. H. Glover, R. L. Goode, E. V. Sullivan and J. D. E. Gabrieli (1998). "Sniffing and smelling: separate subsystems in the human olfactory cortex". Nature (392): 282–286.  Cite uses deprecated parameter |coauthors= (help)
  10. ↑ 10.0 10.1 Vanderwolf, C. H. (2001). "The hippocampus as an olfacto-motor mechanism: were the classical anatomists right after all?". Behav Brain Res (127): 25–47. 
  11. ↑ 11.0 11.1 Johnson, B. N.; Mainland, J. D. & Sobel, N. (2003). "Rapid olfactory processing implicates subcortical control of an olfactomotor system". J Neurophysiol (90): 1084–1094.  Cite uses deprecated parameter |coauthors= (help)
  12. ↑ 12.0 12.1 Uchida, N.; Kepecs, A. & Mainen, Z. F. (2006). "Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making". Nat Rev Neurosci (7): 485–491.  Cite uses deprecated parameter |coauthors= (help)
  13. ↑ 13.0 13.1 Deschenes, M.; Moore, J. & Kleinfeld, D. (2011). "Sniffing and whisking in rodents". Current Opinion in Neurobiology (22): 1–8.  Cite uses deprecated parameter |coauthors= (help)
  14. ↑ 14.0 14.1 Sobel, N; Thomason, M.E, Stappen, I., Tanner, C. M., Tetrud, J. W., Bower, J. M., Sullivan, E. V., and Gabrieli, J. D. E. (2001). "An impairment in sniffing contributes to the olfactory impairment in Parkinson's disease". Proc Natl Acad Sci U S A (98): 4154–4159.  Cite uses deprecated parameter |coauthors= (help)
  15. ↑ 15.0 15.1 Wesson, D. W.; Varga-Wesson, A. G., Borkowski, A. H. & Wilson, D. A (2011). "Respiratory and sniffing behaviors throughout adulthood and aging in mice". Behavioural Brain Research (223): 99–106.  Cite uses deprecated parameter |coauthors= (help)
  16. ↑ 16.0 16.1 Massengale, O.N.; Glaser, H. H., LeLievre, R. E., Dodds, J. B. & Klogk, M. E. (1963). "Physical and Psychologic Factors in Glue Sniffing". New England Journal of Medicine (269): 1340–1344. doi:10.1056/NEJM196312192692503.  Cite uses deprecated parameter |coauthors= (help)
  17. ↑ 17.0 17.1 Teghtsoonian, R.; Teghtsoonian, M (1982). "Perceived effort in sniffing: The effects of sniff pressure and resistance.". Perception & Psychophysics. 31: 324–329.  Cite uses deprecated parameter |coauthors= (help)
  18. ↑ 18.0 18.1 Wesson, D.W.; Verhagen, J. V. & Wachowiak, M. (2009). "Why Sniff Fast? The Relationship Between Sniff Frequency, Odor Discrimination, and Receptor Neuron Activation in the Rat". J Neurophysiol (101): 1089–1102. doi:10.1152/jn.90981.2008.  Cite uses deprecated parameter |coauthors= (help)
  19. ↑ 19.0 19.1 Dethier, V.G. (1987). "Sniff, Flick, and Pulse: An Appreciation of Interruption". Proceedings of the American Philosophical Society (131): 159–176. 
  20. ↑ 20.0 20.1 Catania, K.C. (2006). "Olfaction: Underwater 'sniffing' by semi-aquatic mammals". Nature (444): 1024–1025. 
  21. ↑ 21.0 21.1 Karpov, A.P. (1980). Neural Mechanisms of Goal-Directed Behavior and Learning. Academic Press. pp. 273–282. 
  22. ↑ 22.0 22.1 Clarke, S. (1971). "Sniffing and fixed-ratio behavior for sucrose and brain stimulation reward in the rat". Physiol Behav (7): 695–699. 
  23. ↑ 23.0 23.1 Jones, F.N. (1955). "The reliability of olfactory thresholds obtained by sniffing". Am J Psychol (68): 289–290. 
  24. ↑ 24.0 24.1 Adrian, E.D. (1942). "Olfactory reactions in the brain of the hedgehog". Journal of Physiology (100): 459–473. 
  25. ↑ 25.0 25.1 Mozell, M.M. (1964). "Evidence for sorption as a mechanism of the olfactory analysis of vapours". Nature (203): 1181–1182. 
  26. ↑ 26.0 26.1 Macrides, F.; Chorover, S. L (1972). "Olfactory bulb units: activity correlated with inhalation cycles and odor quality". Science (175): 84–87.  Cite uses deprecated parameter |coauthors= (help)
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