Odor-associative learning and emotion: effects on perception and behavior.
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Biomedical subjects
Publications and source records attributed to Rachel S Herz.
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STUDY OBJECTIVES: To examine olfactory arousal threshold during sleep in comparison to an auditory tone. DESIGN: On night 1, participants rated odor intensity when awake and experienced olfactory stimuli during stage 1 sleep. Night 2 involved stage 2, stage 4, and rapid-eye-movement (REM) sleep trials using the "staircase" threshold-detection method. Electroencephalogram, electrooculogram, electromyogram, electrocardiogram, and respiration were recorded along with behavioral response. An 800-Hz tone was given on trials when odors failed to arouse. SETTING: Participants slept in individual rooms. Stimulus-delivery systems were operated from a separate room, where an experimenter observed physiologic recordings and behavioral responses. PARTICIPANTS: Three healthy men and 3 women aged 20 to 25 years (mean, 22 years). INTERVENTIONS: Two odorants, peppermint and pyridine, at 4 concentrations were presented through nasal cannulas using an air-dilution olfactometer. Tones were played over a speaker. MEASUREMENTS: Behavioral (button press and oral) responses, electroencephalographic activation, and changes in breathing and heart rate were assessed. RESULTS: Participants responded to odors on 92% of stage 1 sleep trials. Peppermint was ineffective in stages 2, 4, and REM sleep. Pyridine produced behavioral threshold on 45% of stage 2 trials, none in stage 4, and one third of REM sleep trials. Tones were effective on at least 75% of trials. Heart rate increased significantly only following behavioral responses to odors or tones across sleep stages. CONCLUSIONS: The data indicate that human olfaction is not reliably capable of alerting a sleeper.
To assess past behavioral reports of the emotional distinctiveness of odor-evoked memories, functional magnetic resonance imaging (fMRI) was used to compare regions of activation during recall triggered by olfactory and visual cues that were connected to a personally meaningful memory and a comparable control cue presented in olfactory and visual form. Five healthy right-handed females experienced both behavioral and fMRI memory testing. fMRI analyses indicated significantly greater activation in the amygdala and hippocampal regions during recall to the personally significant odor than any other cue, and behavioral responses confirmed that emotional responses were greatest to the personally meaningful odor. These findings provide convincing neurobiological evidence that the subjective experience of the emotional potency of odor-evoked memory is correlated with specific activation in the amygdala during recall and offers new insights into the affective organization of memory.
The emotional and content qualities of autobiographical memories evoked by three memory cue items (campfire, fresh-cut grass, popcorn) presented in olfactory, visual and auditory form were examined using a new repeated measures paradigm. Results revealed that memories recalled by odors were significantly more emotional and evocative than those recalled by the same cue presented visually or auditorily. However, there were no differences in the content features (vividness, specificity) of memories as a function of cue-form. These findings support previous research in both laboratory and naturalistic settings and is the first comparative sensory memory study to include auditory variants of memory cues. The present data contribute to a growing body of evidence indicating that there is a privileged relationship between olfaction and emotion during recollection. Various subject factors such as age, sex and region of residence were also examined and some were found to affect the quality of memories in interaction with the specific memory cue items, indicating that prior experience is a primary influence in autobiographical memory. Questions for future investigation regarding how odor-evoked memories may be different from other memory experiences are suggested.
Three experiments were conducted to examine how verbal context and sensory stimulation interact to influence odor hedonic perception. Eight common odors were presented in their natural and synthetic forms, and verbal labels designating name and source (natural, synthetic) information were either explicitly given, self-generated, falsely provided, or not provided. Results revealed that verbal information about source influenced hedonic ratings whether or not the odorant itself was also present. When odorants were presented without verbal labels, olfactory evaluations were based in sensation. Name and source information contributed different levels of meaning and influence to perceptual evaluations. The findings are discussed with reference to an experiential-collocation model for odor-label interactions and a dual-coding hypothesis for olfactory perception.
The emotional and evocative qualities of autobiographical memories evoked by odors and visual cues were compared using a new repeated-measures paradigm in which the sensory cue was presented after the memory had been retrieved by its verbal label. Memory cues were chosen to be able to elicit salient memories. Results revealed that memories recalled in the context of odors were significantly more emotional than those recalled in the context of the same cue presented visually and by the verbal label for the cue. Odor-evoked memories also tended to make participants feel more "brought back" to the original event. This work is the first unequivocal demonstration that naturalistic memories evoked by odors are more emotional than memories evoked by other cues.