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Featured ArticleArticles, Behavioral/Cognitive

Olfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior

Anat Arzi, Yael Holtzman, Perry Samnon, Neetai Eshel, Edo Harel and Noam Sobel
Journal of Neuroscience 12 November 2014, 34 (46) 15382-15393; https://doi.org/10.1523/JNEUROSCI.2291-14.2014
Anat Arzi
Department of Neurobiology, Weizmann Institute of Science, Rehovot, 7610001 Israel
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Yael Holtzman
Department of Neurobiology, Weizmann Institute of Science, Rehovot, 7610001 Israel
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Perry Samnon
Department of Neurobiology, Weizmann Institute of Science, Rehovot, 7610001 Israel
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Neetai Eshel
Department of Neurobiology, Weizmann Institute of Science, Rehovot, 7610001 Israel
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Edo Harel
Department of Neurobiology, Weizmann Institute of Science, Rehovot, 7610001 Israel
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Noam Sobel
Department of Neurobiology, Weizmann Institute of Science, Rehovot, 7610001 Israel
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  • Figure 1.
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    Figure 1.

    Experimental protocols. A, Experimental time line. B, Experimental setup. Top left, The olfactometer (odor generating device). Bottom left, A subject with polysomnography devices and nasal mask for odor administration with pneumotachograph for precise sniff recording. Right, Polysomnography and respiration recording. The experimenter manually initiated odor onset according to the desired sleep stage, REM sleep in this case. Ci, The main experimental protocol. Olfactory partial-reinforcement aversive trace conditioning between cigarette odor (Cig) and unpleasant odors. Stimuli were generated in blocks of 30 trials: 10 reinforced trials with unpleasant AmSu odor (AS; yellow), 10 reinforced trials with unpleasant RF odor (brown) and 10 nonreinforced trials (cigarette odor alone; gray). Cii, The control protocol of unpleasant odors alone. Unpleasant odor administration in the same experimental procedure as in A, yet cigarette odor was replaced with clean air. Ciii, The nonconditioned control protocol. Cigarette and unpleasant odor administration in randomized order such that the cigarette odor and unpleasant odors were nonconditioned.

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    Figure 2.

    Odors were unpleasant as intended. Odorant ranking on a visual analog scale (145 mm long). A, Pleasantness ranking ranging from very unpleasant (0) to very pleasant (145). The dotted line denotes neutral valence. B, Intensity ranking ranging from very weak (0) to very strong (145). ***p < 0.0005.

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    Figure 3.

    Odors did not awaken subjects. A–C, EEG spectral analysis of 20 s after odor onset in the δ, θ, α, σ, and β frequency band following (A) RF, (B) AmSu, and (C) cigarette odor. *p < 0.05, #p = 0.08.

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    Figure 4.

    Unpleasant odors reduced first sniff duration during sleep. Normalized sniff duration for three consecutive sniffs following unpleasant odors (black) and cigarette odor (gray) during sleep. The first sniff following unpleasant odor onset was significantly shorter compared with baseline, implying that the sleeping brain indeed registered odor presence and quality. *p < 0.05.

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    Figure 5.

    Aversive conditioning during sleep reduced subsequent smoking. A, Number of smoked cigarettes at baseline and in each day following olfactory aversive conditioning during stage 2 sleep (black), REM sleep (dark gray), and wake (outline). B, Percentage change in smoked cigarettes in the first half (days 1–3) and second half (days 5–7) of the experiment following conditioning during stage 2 sleep (black), REM sleep (dark gray), and wake (outline). C, D, Intercept (C) denoting the effect size of the change in smoked cigarettes and slope (D) denoting the change in smoked cigarettes across 7 PE days, following olfactory aversive conditioning during stage 2 sleep (black), REM sleep (dark gray), and wake (outline). *p < 0.05, **p < 0.01, ***p < 0.005.

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    Figure 6.

    Olfactory aversive conditioning reduced smoking more effectively than unpleasant odors alone. A, Number of smoked cigarettes at baseline and in each day following olfactory aversive conditioning (black) and unpleasant odor (light gray) administration in sleep (stage 2 and REM combined). B, Percentage change in smoked cigarettes in the first half (days 1–3) and second half (days 5–7) of the experiment following olfactory aversive conditioning (black) and unpleasant odors alone (light gray). C, D, Intercept (C) denoting the effect size of the change in smoked cigarettes and slope (D) denoting the change in smoked cigarettes across 7 PE days following olfactory aversive conditioning (black) and unpleasant odors alone (light gray). *p < 0.05, **p < 0.01, ***p < 0.005.

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    Figure 7.

    Olfactory aversive conditioning reduced smoking more effectively than nonconditioned odors. A, Number of smoked cigarettes at baseline and in each day following olfactory aversive conditioning (black) and nonconditioned odor (striped) administration during stage 2 sleep. B, Percentage change in smoked cigarettes in the first half (days 1–3) and second half (days 5–7) of the experiment following olfactory aversive conditioning (black) and nonconditioned odor (striped) administration during stage 2 sleep. C, D, Intercept (C) denoting the effect size of the change in smoked cigarettes and slope (D) denoting the change in smoked cigarettes across 7 PE days following olfactory aversive conditioning (black) and nonconditioned odor (striped) administration during stage 2 sleep. *p < 0.05, **p < 0.01, ***p < 0.005.

Tables

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    Table 1.

    Sleep architecture

    REM groupStage 2 groupt(1,22)p
    Wake after sleep onset (%)15.32 ± 8.3412.29 ± 6.780.98>0.34
    Stage 1 sleep (%)3.76 ± 5.673.53 ± 5.970.09>0.93
    Stage 2 sleep (%)51.03 ± 8.3451.39 ± 7.620.11>0.91
    SWS (%)15.97 ± 7.6119.07 ± 6.821.05>0.30
    REM sleep (%)13.92 ± 3.9213.70 ± 7.700.09>0.93
    Total sleep time (min)368.95 ± 56.19346.53 ± 48.940.78>0.44
    Latency from sleep onset to first trial onset (min)198.52 ± 74.52185.37 ± 17.370.60>0.56
    Number of trials25.50 ± 6.5427.42 ± 4.540.83>0.41
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The Journal of Neuroscience: 34 (46)
Journal of Neuroscience
Vol. 34, Issue 46
12 Nov 2014
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Olfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior
Anat Arzi, Yael Holtzman, Perry Samnon, Neetai Eshel, Edo Harel, Noam Sobel
Journal of Neuroscience 12 November 2014, 34 (46) 15382-15393; DOI: 10.1523/JNEUROSCI.2291-14.2014

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Olfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior
Anat Arzi, Yael Holtzman, Perry Samnon, Neetai Eshel, Edo Harel, Noam Sobel
Journal of Neuroscience 12 November 2014, 34 (46) 15382-15393; DOI: 10.1523/JNEUROSCI.2291-14.2014
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Keywords

  • aversive conditioning
  • olfaction
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