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Coordination of sniffing and whisking depends on the mode of interaction with the environment

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Smell and touch convey most of the information that nocturnal rodents collect in their natural environments, each via its own complex network of muscles, receptors and neurons. Being active senses, a critical factor determining the integration of their sensations relates to the degree of their coordination. While it has been known for nearly 50 years that sniffing and whisking can be coordinated, the dynamics of such coordination and its dependency on behavioral and environmental conditions are not yet understood. Here we introduce a novel non-invasive method to track sniffing along with whisking and locomotion using high-resolution video recordings of mice, during free exploration of an open arena. Active sensing parameters in each modality showed significant dependency on exploratory modes (“Outbound”, “Exploration” and “Inbound”) and locomotion speed. Surprisingly, the correlation between sniffing and whisking was often as high as the bilateral inter-whisker correlation. Both inter-whisker and inter-modal coordination switched between distinct high-correlation and low-correlation states. The fraction of time with high-correlation states was higher in the Outbound and Exploration modes compared with the Inbound mode. Overall, these data indicate that sniffing–whisking coordination is a complex dynamic process, likely to be controlled by multiple-level inter-modal coordinated loops of motor-sensory networks.

Affiliations: 1: Department of Physics of Complex Systems, Weizmann Institute of Science ehud.fonio@weizmann.ac.il ; 2: Department of Industrial Engineering, Tel-Aviv University ; 3: Department of Neurobiology, Weizmann Institute of Science ; 4: Department of Structural Biology, Stanford University

10.1080/15659801.2015.1124656
/content/journals/10.1080/15659801.2015.1124656
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1. Ahissar E,, Kleinfeld D. 2003. "Closed-loop neuronal computations: focus on vibrissa somatosensation in rat". Cereb Cortex. Vol 13:5362.
2. Angelaki DE,, Gu Y,, DeAngelis GC. 2009. "Multisensory integration: psychophysics, neurophysiology, and computation". Curr Opin Neurobiol. Vol 19:452458.
3. Arkley K,, Grant RA,, Mitchinson B,, Prescott TJ. 2014. "Strategy change in vibrissal active sensing during rat locomotion". Curr Biol. Vol 24:15071512.
4. Berg RW,, Kleinfeld D. 2003. "Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control". J Neurophysiol. Vol 89:104117.
5. Cao Y,, Roy S,, Sachdev RN,, Heck DH. 2012. "Dynamic correlation between whisking and breathing rhythms in mice". J Neurosci. Vol 32:16531659.
6. Deschênes M,, Haidarliu S,, Demers M,, Moore J,, Kleinfeld D,, Ahissar E. 2014. "Muscles involved in naris dilation and nose motion in rat". Anat Rec. Vol 298:546553.
7. Deschênes M,, Moore J,, Kleinfeld D. 2012. "Sniffing and whisking in rodents". Curr Opin Neurobiol. Vol 22:243250.
8. Deutsch D.,, Pietr M,, Knutsen PM,, Ahissar E,, Schneidman E. 2012. "Fast" "feedback in active sensing: touch-induced changes to whisker-object interaction". PLOS One Vol 7:e44272.
9. Eilam D,, Golani I. 1989. "Home base behavior of rats Rattus norvegicus exploring a novel environment". Behav Brain Res. Vol 34:199211.
10. Ernst MO,, Banks MS. 2002. "Humans integrate visual and haptic information in a statistically optimal fashion". Nature Vol 415:429433.
11. Fonio E,, Benjamini Y,, Golani I. 2009. "Freedom of movement and the stability of its unfolding in free exploration of mice". Proc Natl Acad Sci USA. Dec;Vol 106:2133521340. Epub 2009 Nov 26.
12. Gao P,, Bermejo R,, Zeigler HP. 2001. "Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator". J Neurosci. Vol 21:53745380.
13. Golani I,, Benjamini Y,, Eilam D. 1993. "Stopping behavior: constraints on exploration in rats Rattus norvegicus". Behav Brain Res. Vol 53:2133.
14. Gordon G,, Fonio E,, Ahissar E. 2014. "Emergent exploration via novelty management". J Neurosci. Vol 34:1264612661.
15. Grant RA,, Mitchinson B,, Fox CW,, Prescott TJ. 2009. "Active touch sensing in the rat: anticipatory and regulatory control of whisker movements during surface exploration". J Neurophysiol. Feb;Vol 101:862874. Epub 2008 Nov 28.
16. Haidarliu S,, Ahissar E. 2001. "Size gradients of barreloids in the rat thalamus". J Comp Neurol. Vol 429:372387.
17. Haidarliu S, Kleinfeld D, Deschênes M, Ahissar E. 2015. The musculature that drives active touch by vibrissae and nose in mice. Anat Rec. 298:1347–1358.
18. Hill DN, Bermejo R, Zeigler HP, Kleinfeld D. 2008. Biomechanics of the vibrissa motor plant in rat: Rhythmic whisking consists of triphasic neuromuscular activity. J Neurosci. 2008;28:3438–3455.
19. Hillis JM,, Ernst MO,, Banks MS,, Landy MS. 2002. "Combining sensory information: mandatory fusion within, but not between, senses". Science Vol 298:16271630.
20. Jacobs RA. 1999. "Optimal integration of texture and motion cues to depth". Vis Res. Vol 39:36213629.
21. Kepecs A,, Uchida N,, Mainen ZF. 2007. "Rapid and precise control of sniffing during olfactory discrimination in rats". J Neurophysiol. Vol 98:205213.
22. Knutsen PM,, Pietr M,, Ahissar E. 2006. "Haptic object localization in the vibrissal system: behavior and performance". J Neurosci. Aug;Vol 26:84518464. Epub 2006 Aug 18.
23. Koelewijn T,, Bronkhorst A,, Theeuwes J. 2010. "Attention and the multiple stages of multisensory integration: a review of audiovisual studies". Acta psychologica. Vol 134:372384.
24. Körding KP, Wolpert DM. 2004. Bayesian integration in sensorimotor learning. Nature 427:244–247.
25. Macrides F,, Eichenbaum HB,, Forbes WB. 1982. "Temporal relationship between sniffing and the limbic rhythm during odor discrimination reversal learning". J Neurosci. Vol 2:17051717.
26. Mitchinson B,, Martin CJ,, Grant RA,, Prescott TJ. 2007. "Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact". Proc Biol Sci. Apr.Vol 274:10351041. Epub 2007 Mar 03.
27. Moore JD,, Deschênes M,, Furuta T,, Huber D,, Smear MC,, Demers M,, Kleinfeld D. 2013. "Hierarchy of orofacial rhythms revealed through whisking and breathing". Nature.Vol 497:205210.
28. Moore JD,, Kleinfeld D,, Wang F. 2014. "How" "the brainstem controls orofacial behaviors comprised of rhythmic actions". Trends Neurosci. 37:370–380.
29. Perkon I,, Kosir A,, Itskov PM,, Tasic JF,, Diamond ME. 2011. "Unsupervised" "quantification of whisking and head movement in freely moving rodents". J Neurophysiol. 105:1950–1962.
30. Ranade S,, Hangya B,, Kepecs A. 2013. "Multiple modes of phase locking between sniffing and whisking during active exploration". J Neurosci. Vol 33:82508256.
31. Saig A,, Gordon G,, Assa E,, Arieli A,, Ahissar E. 2012. "Motor-sensory confluence in tactile perception". J Neurosci. Vol 32:1402214032.
32. Semba K,, Komisaruk BR. 1984. "Neural substrates of two different rhythmical vibrissal movements in the rat". Neuroscience. Jul;Vol 12:761774. Epub 1984 Jul 01.
33. Tchernichovski O,, Benjamini Y,, Golani I. 1998. "The dynamics of long-term exploration in the rat. Part I. A phase-plane analysis of the relationship between location and velocity". Biol Cybern. Jun;Vol 78:423432. Epub 1998 Aug 26.
34. Tchernichovski O,, Golani I. 1995. "A phase plane representation of rat exploratory behavior". J Neurosci Methods. Vol 62:2127.
35. Uchida N,, Mainen ZF. 2003. "Speed and accuracy of olfactory discrimination in the rat". Nat Neurosci. Vol 6:12241229.
36. Von Uexküll, J. (1957). A stroll through the worlds of animals and men: A picture book of invisible worlds. In CH Schiller, editor. Instinctive behavior: The development of a modern concept. New York: International Universities Press; p. 5–80. (Original work published 1934).
37. van Beers RJ,, Sittig AC,, Gon JJ. 1999. "Integration of proprioceptive and visual position-information: an experimentally supported model". J Neurophysiol. Vol 81:13551364.
38. Verhagen JV Wesson DW, Netoff TI, White JA, Wachowiak M. 2007. "Sniffing" "controls an adaptive filter of sensory input to the olfactory bulb". Nat Neurosci. Vol 10:631639.
39. Vincent, S. 1912. The function of the vibrissae in the behavior of the white rat. In: Behavior monographs, Vol. 1, Series 5. Chicago: University of Chicago; p. 1–81.
40. Welker WI. 1964. "Analysis of sniffing of the albino rat". Behaviour. Vol 22:223244.
41. Wesson DW,, Carey RM,, Verhagen JV,, Wachowiak M. 2008. "Rapid encoding and perception of novel odors in the rat". PLOS Biol. Vol 6:e82.
42. Wong-Riley MTT. 1979. "Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry". Brain Res. Vol 171:1128.
43. Zuo Y, Perkon I, Diamond ME. 2011. Whisking and whisker kinematics during a texture classification task. Phil. Trans. R. Soc. B. 366:3058–3069.
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/content/journals/10.1080/15659801.2015.1124656
2015-05-05
2018-10-22

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