Cited by 17Memory and Neural MechanismsOlfactory and Sensory Function StudiesNeurotransmitter Receptor Influence on Behavior

Odour conditioning of positive affective states: Rats can learn to associate an odour with being tickled.

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Bombail, Vincent, Jerôme, Nathalie, Lam, Ho, Muszlak, Sacha, Meddle, Simone L., Lawrence, Alistair B., Nielsen, Birte L.·2019·PLOS ONE

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Abstract

Most associative learning tests in rodents use negative stimuli, such as electric shocks. We investigated if young rats can learn to associate the presence of an odour with the experience of being tickled (i.e. using an experimenter's hand to mimic rough-and-tumble play), shown to elicit 50 kHz ultrasonic vocalisations (USVs), which are indicative of positive affect. Male, pair-housed Wistar rats (N = 24) were all exposed to two neutral odours (A and B) presented in a perforated container on alternate days in a test arena. Following 60s of exposure, the rats were either tickled on days when odour A (n = 8) or odour B (n = 8) was present, or never tickled (n = 8). When tickled, rats produced significantly more 50 kHz USVs compared to the days when not being tickled, and compared to control rats. The level of anticipatory 50 kHz USVs in the 60s prior to tickling did not differ significantly between the tickled and control rats. As a retrieval test following the odour conditioning, rats were exposed successively in the same arena to three odours: an unknown neutral odour, extract of fox faeces, and either odours A or B. Compared to controls, 50 kHz USVs of tickled rats increased when exposed to the odour they had previously experienced when tickled, indicating that these rats had learned to associate the odour with the positive experience of being tickled. In a test with free access for 5 min to both arms of a T-maze, each containing one of the odours, rats tickled with odour A spent more time in the arm with this odour. This work is the first to test in a fully balanced design whether rats can learn to associate an odour with tickling, and indicates that positive odour conditioning has potential to be used as an alternative to negative conditioning tests.

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Crossref · 10.1371/journal.pone.0212829

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  • Wistar rats have been shown to be reliably responsive to tickling and PH.

    “This outbred albino strain has been shown to be reliably responsive to tickling and PH ( Bombail et al., 2019; Hammond et al., 2019) and is one of the commonly used strains for such experiments (23% of rat tickling studies used Wistar rats; LaFollette et al., 2017).”

    From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Bombail et al., 2019

    Materials and methods (Animals and housing; page unavailable) identifies the subjects as Wistar rats. The Results report that all tickled rats emitted significantly more 50 kHz vocalisations when tickled, supporting responsiveness to tickling. The tickling procedure included play with the rats, but the paper does not test responsiveness to PH as a separate procedure. (LLM, conf=0.82)

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  • By the 5th session, all PH rats showed an increase in USV production in contrast to the standard protocol where some rats show little or no increase in USVs.

    “By the 5th session, all PH rats showed an increase in USV production in contrast to Figure 2(ii), which used the standard protocol and where some rats show little or no increase in USVs.”

    From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Bombail et al., 2019

    The Results (page not available) report higher average 50 kHz USV production in the fifth than the first tickling session and note individual differences, but do not establish that some rats had little or no increase. The General discussion (page not available) explicitly says the authors did not standardise their tickling method, so this paper does not support describing its procedure as the standard protocol. The statement about all PH rats appears to describe the citing study’s own results, not a finding attributed to this source. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • The PH protocol resulted in a more uniform increase in USVs across individuals relative to the standard protocol.

    “Our data suggest that the PH protocol resulted in a more uniform increase in USVs across individuals relative to the standard protocol.”

    From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Bombail et al., 2019

    In the General discussion (page unavailable), the authors say that adapting tickling to each rat appeared to reduce individual variation in responses compared with a standardized approach. They do not report a comparison showing that a PH protocol produced a more uniform increase in USVs than a standard protocol; the Results instead report that USV response levels varied by individual rat. (LLM, conf=0.83)

    Experimental — accuracy not yet measured
  • The PH protocol is intended to better mimic the dynamic nature of play, giving the rat more choice over how it is tickled.

    “Due to our experiences using the standard tickling protocol we have developed a refined tickling protocol we refer to as playful handling (PH), intended to better mimic the dynamic nature of play, giving the rat more choice over how it is tickled ( Bombail et al., 2019), Figure 1(iii).”

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Research works printed but not linked: 2

  1. [9]Deehan GA Jr, Ding Z-M, Hauser SR, Engleman EA, Wilden JA, McBride WJ, et al Conditioned odor cues associated with the access to or the absence of alcohol differentially modulate dopmamine efflux in the nucleus accumbens shell. Alcohol Clin Exp Res. 2012; 36: 186A.
  2. [36]Lam H. Can odour be associated with positive affective states in rats (Rattus norvegicus)? MSc thesis, University of Edinburgh; 2017. 45 pp.

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Authors
Bombail, V., Jerôme, N., Lam, H., Muszlak, S., Meddle, S. L., Lawrence, A. B., & Nielsen, B. L.
Affiliations
  • Université Paris-Saclay (FR)
  • Roslin Institute (GB)
  • AgroParisTech (FR)
Venue
PLOS ONE
Published
2019-06-12
Volume
14
Issue
6
Pages
e0212829
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2949794481
Cited by
17
References
49
Citations by year
2026: 2 · 2025: 2 · 2024: 1 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 1 · 2019: 1
FWCI
1.16
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders
  • RESAS
  • Biotechnology and Biological Sciences Research Council
  • Department of Animal Physiology and Livestock Systems
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
positive affective states, tickling, associative learning, rats, rough-and-tumble play
MeSH terms
Animals, Conditioning, Psychological, Learning, Male, Odorants, Physical Stimulation, Ultrasonics, Rats, Wistar, Rats

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