Unhealthy behaviours trigger brain responses that are similar to those prompted by bad smells


Unhealthy behaviours trigger moral judgments that are similar to the basic emotions that contribute to our ability to survive.

Two different hypotheses are to be found in the current scientific literature as to the identity of these emotions. Some researchers single out disgust, while others opt for pain.

After developing a new approach to brain imaging, a research team from the University of Geneva (UNIGE) has come down on the side of disgust.

The study, which can be found in Science Advances, shows that unhealthy behaviours trigger brain responses that are similar to those prompted by bad smells. The research also identifies for the first time a biomarker in the brain for disgust.

Disgust is a basic emotion linked to our survivability. Smell provides information about the freshness of foodstuffs, while disgust means we can take action to avoid a potential source of poisoning.

Following the same principle, pain helps us cope with any injuries we might suffer by activating our withdrawal reflexes. Psychologists believe that these types of survival reflexes might come into play in response to other people’s bad behaviour.

Disgust or pain

“These connections have been demonstrated via associations between situations and sensations,” begins Professor Corrado Corradi-Dell’Acqua, a researcher in UNIGE’s Department of Psychology and the study’s lead investigator.

“For instance, if I drink something while reading an article about corruption that affects my moral judgment, I may find that my drink smells bad and tastes vile.

Equally, the reverse is true: smells can generate inappropriate moral judgment.

In concrete terms, if someone smells bad, other people tend to make the judgment that they’re unhealthy.”

While some studies suggest that disgust is involved in the process, others opt for pain, since they consider that moral judgments are made based on actual facts – hence the parallel with the mechanisms involved in pain.

“If a driver is distracted, and does not see a pedestrian crossing a road, I will judge this person more negatively if the pedestrian was actually harmed, rather than avoided by chance”, explains the psychologist. His team set up an experimental paradigm and customised magnetic resonance imaging (MRI) techniques in an attempt to decide between the contradictory hypotheses.

The train dilemma as a paradigm

The first step was for Corradi-Dell’Acqua’s laboratory to subject volunteers to unpleasant odours or heat-induced pain.

“The whole idea was to elicit a similar degree of discomfort with the two techniques so that they could work on the same levels.” Once the calibration had been performed, participants in the study were subjected to readings that evoked value judgments.

“We used the train dilemma when five people are stuck on a railway track as a train approaches. The only possible way to save them is to push someone off the top of a bridge so that the switch is hit as they fall. In other words, it’s necessary to kill one person to save five in a highly immoral situation,” explains the researcher.

This shows brain scans from the study
Part of the human brain contributing the most to the prediction of pain and olfactory disgust.

The act of reading this unpleasant dilemma had an influence on the odours the participants smelt and caused disgust, but did not influence the pain, an outcome that was backed up by the participants’ electrodermal activity.

This is a physiological measurement of the electrical conductance of the skin. It reflects the rate of sweating and the activity of the nervous system responsible for involuntary behaviour.

Neural pathways identified

Professor Corradi-Dell’Acqua then concentrated on the brain response. “It is difficult to infer pain and disgust from neural activity, as these two experiences often recruit the same brain areas.

To dissociate them, we had to measure the global neuronal activity via MRI rather than focusing on specific regions,” summarises the researcher. The Geneva team adopted a technique that allows predicting disgust and pain from the overall brain activity, such as specific biomarkers.

Using this tool, the researchers were able to prove that the overall brain response to disgust was influenced by previous moral judgment. Once again, moral judgments are indeed associated with disgust.

“In addition to this important discovery for psychology, this study was the occasion for the development of a biomarker prototype for olfactory disgust. It’s a double step forward!” concludes Corradi-Dell’Acqua.

Odor memory is a central feature of olfactory cognition, and can be divided into two distinct cognitive-perceptual processes [1,2,3]. One is the ability to recognize and remember whether one has smelled an odor before. This form of odor memory is similar to recognizing other sensory semantic cues, such as knowing that a particular sound signifies your dog’s bark.

Odor recognition and identification, and in particular its failure, is a critical factor in human health. Data from a representative sample of over 3000 US community dwelling adults 57 years and older, recently revealed that those who were dysfunctional at odor identification were four times more likely to die within a five year period than their same age peers with normal olfactory abilities [4].

Impairment of odor identification is also a hallmark early symptom and predictor of several neurological disorders, most notably Alzheimer’s disease and Parkinson’s disease.

For recent reviews of these topics see Doty [5] and Velayudhan [6]. The second type of odor memory is odor-evoked memory—autobiographical memories and associations that are triggered by odors. This type of memory has not been directly examined for the ways in which it may be involved in human health, and an effort to do so is the subject of the present article.

Odor-evoked memory or the “Proust phenomenon” [7] from the eponymous literary anecdote where Marcel Proust took a bite of madeleine biscuit that had been dipped in Linden tea and was suddenly transported to a long forgotten moment in his childhood [8], occurs when an odor triggers the recollection of a meaningful past personal episode.

Odor-evoked memories possess several characteristics that distinguish them from memories evoked by stimuli perceived through other sensory modalities (for reviews see [2,9]. Notably, odor-evoked memories have been shown to be more rare, less frequently thought about [10,11,12], and from an earlier time in life, specifically clustered in the first decade [10,12,13] compared with memories evoked by verbal or visual stimuli.

The most distinctive characteristics of odor-evoked memories, however, and why they are important to human health and wellbeing is that they evoke more emotional and evocative recollections than memories triggered by any other cue.

Numerous studies have now shown that autobiographical memories triggered by odors feel much more emotional, activate the neurolobiological substrates of emotional processing, and that people are more brought to the original time and place of their memories compared to when the same events are recalled through other modalities [12,14,15,16,17,18,19,20].

Odor-evoked memories are exceptionally viscerally involving because the neuroanatomy of olfaction has a privileged and unique connection to the neural substrates of emotion and associative learning. The primary olfactory cortex includes the amygdala, which processes emotional experience and emotional memory, as well as the hippocampus, which is involved in associative learning [21,22,23,24].

Thus, the mere act of smelling activates the amydala-hippocampal complex. Moreover, during the process of recollecting an odor-evoked autobiographical memory, the amygdala is more activated than when similar odors that do not evoke a memory are smelled [18].

Additionally, the secondary olfactory cortex (the orbitofrontal cortex) is the cortical area responsible for assigning affective value to stimuli and for determining the reinforcement value of stimuli in general [25,26].

Finally, unlike other sensory systems where neural processing is directly integrated in the thalamus prior to processing in the cortex [27], olfactory information is indirectly processed through the medio-dorsal nucleus of the thalamus which appears to play a role in modulating attention to odors [27,28,29], and the primary processing of odors occurs instead in the amygdala-hippocampal complex of the limbic system. None of our other senses have this level of targeted connection with the areas of the brain that process emotion, associative learning, and memory.

The present review will explain how through their uniquely emotional and evocative properties odor-evoked memories alter mood and induce the physical correlates of various emotional states, and thus that they are important to, and can be used for, ameliorating psychological and physical health.

The following two sections discuss recent research where odor-evoked memories have been found to affect emotional and physiological responses and the implications these findings have for human health. Olfactory factors and individual difference characteristics that would need to be considered in any therapeutic application of odor-evoked are then examined.

The paper concludes with a discussion of the mechanisms through which odor-evoked memories exert their positive effects and offers some directions for future research that are now needed in order to mine the therapeutic potential of odor-evoked memory. Table 1 provides a synopsis of the methods and results of the relevant odor-evoked memory studies reviewed here.

Table 1

Methods and results in odor-evoked memory research with implications for psychological and physiological health.

Studies Reporting Predominantly Psychological Effects
Arshamanian et al., 2013 [10]Familiar odors evocative of an AM were compared with memories elicited by verbal labels for those odors during fMRI scanning. Post-scanning, odors and labels were re-assessed and participants provided subjective evaluations of their memories.Odors elicited more emotional and positive memories, and more activity in parahippocampal, amygdala and tempopolar regions than labels.
Miles and Bernsten (2011) [13]12 familiar stimuli presented in verbal, visual and olfactory formats were compared for various qualitative dimensions of memory.Odor-evoked memories were more positive, and more relevant to one’s life story than memories elicited by verbal or visual cues.
Reid et al. (2015) [32]12 common scents were evaluated for nostalgic evocation and associated feelings.Higher levels of odor-evoked nostalgia elicited higher levels of positive affect, self-esteem, self and social connectedness, optimism, and life meaning. Nostalgic scents elicited 3× more positive than negative emotions, and 2× more positive emotions than in a previous study examining music-evoked nostalgia.
Toffolo et al. (2012) [33]An aversive documentary was paired with an olfactory, visual or auditory cue. One week later memories for the documentary were compared.The olfactory condition elicited more arousing, detailed and unpleasant memories of the documentary than the auditory condition.
Willander and Larsson (2007) [20]10 common scents were presented in odor-only, verbal-only, and odor + verbal format as memory cues and various experiential factors were assessed.Odor-only cues elicited the most positive, emotional, and evocative memories.
Vermetten and Bremner (2003) [34]Case reports of three individuals suffering from odor-evoked PTSD.Odors specific to a given individual’s past trauma evoked PTSD flashbacks that were intensely negative, persisted for decades, and did not extinguish with time.
Studies Reporting Predominantly Physiological Effects
Masaoka et al., 2012 [35]A self-selected perfume that evoked an AM for each participant was compared to pleasant/neutral CFs.Odors that evoked AMs promoted deeper, slower and more relaxed breathing compared to the CFs. More evocative memories and deeper breathing was observed among individuals who scored highest in trait anxiety.
Matsunaga et al. (2011) [36]A self-selected perfume that evoked an AM for each participant was compared to a pleasant unfamiliar CF. Evoked emotions and associations were evaluated using rating scales. HR, SC, and plasma IL-2 levels in response to the odors were measured.AM fragrances elicited more positive emotion, increased feelings of comfort and happiness, and decreased anxiety compared to the CF. HR decreased, SC increased, and IL-2 decreased after smelling the AM compared to the cf.
Matsunaga et al. (2013) [37]A self-selected fragrance that evoked an AM for each participant was compared to two pleasant generic CFs. Emotions and memories evoked were evaluated. Plasma TNF-α, IFN-γ and IL levels in response to the odors were measured. PET scans of neurological activity during odor exposure were assessed.6.5 times more feelings of nostalgia was experienced to the AM than CF. TNF-α and IFN-γ were decreased after smelling the AM. mOFC and precuneus/PCC were significantly activated during AMs, and activity in the mOFC and precuneus/PCC were negatively correlated with IFN-γ concentration. No IL changes were observed.
Sayette & Parrot (1999) [38]Chronic smokers sniffed either a pleasant odor, an unpleasant odor, or a no-odor control when they experienced a cigarette craving.Sniffing odors reduced cravings for cigarettes compared to the control condition. There was a trend for odors that evoked a memory to be the most effective at diminishing urges.
AM = autobiographical memory; CF = control fragrance; HR = heart-rate; SC = skin conductance; PTSD = post-traumatic stress disorder; IL = interleukin; TNF = tumor necrosis factor; IFN = interferon; PCC = posterior cingulate cortex; mOFC = medial orbitofrontal cortex.

Odor-Evoked Memory and Psychological Responses

Positive moods and emotions are known to be beneficial for psychological health [30] and odor-evoked memories have been shown to be more positive than memories elicited by other cues. Willander and Larsson [20] compared memories evoked by odors, verbal labels, and odors + labels in healthy older adults and found that memories evoked by odors were significantly more pleasant than memories evoked by labels.

Additionally, Arshamian and colleagues [14] found that among male and female adults (age range 20–28 years) autobiographical memories elicited by odors were more emotionally intense and positive than memories cued by verbal labels for the same odors. Arshamian et al. [14] also showed that odor-evoked memories were associated with more activity in the temporal gyrus and temporal pole than verbally evoked memories.

The temporal poles have been linked to the processing of pleasant memories [31], therefore Arshamian et al. [14] speculated that increased temporal pole activity may underlie the superior positively of odor-evoked-memories.

Pleasant autobiographical memories in general can induce positive mood, and invoking such memories has been used as a therapeutic technique to repair emotional distress in various clinical conditions [39,40]. Since odors elicit more emotional memories than other types of stimuli, and because odor-evoked memories tend to be positive, odors may be especially helpful for enhancing mood states.

Indeed, Matsunaga et al. [36] found that when men and women aged 21–38 were presented with the scent of a perfume that was personally reminiscent for them, more positive emotion, increased moods of comfort and happiness, and a decrease in anxiety were experienced compared to when a pleasant fragrance that did not elicit personal memories was presented.

Beyond the specificity of memory, nostalgia—reflecting upon one’s personal past—has been shown to have many beneficial psychological consequences. Engaging in nostalgic reminiscence increases positive affect, bolsters self-esteem, strengthens the connection between one’s past and present, produces feelings of social connectedness, elevates optimism, and infuses life with meaning (see [32] for a review). Recent research suggests that odor-evoked memories may be especially nostalgic triggers.

Matsunaga et al. [37] found that among young adults, odors that evoked personal memories elicited approximately 6.5 times more feelings of nostalgia than odors that did not evoke a specific past event.

Moreover, a comparison of music-evoked nostalgia with odor-evoked nostalgia showed that odors elicited more than twice as many nostalgic reveries as musical excepts did [32,41].

This is an important finding since music is renowned as an emotionally evocative stimulus and it is often reported that music evokes poignant memories [42]. Further support for the nostalgic power of odors was shown by Miles and Bernsten [13] who presented 12 familiar stimuli (e.g., mustard, coffee) in verbal, visual and olfactory formats to a large sample of female college students and compared various qualitative dimensions of memory.

They found that memories evoked by odors were judged as more relevant to one’s life story than memories elicited by verbal or visual cues.

Reid et al. [32] recently performed an in-depth analysis of odor-evoked nostalgia with college students using 12 common scents and demonstrated that, consistent with the beneficial effects of nostalgia in general, high levels of odor-evoked nostalgia were associated with high levels of positive affect, self-esteem, self and social connectedness, optimism, and life meaning.

Reid et al. [32] also found that nostalgic scents elicited three times more positive emotions than negative emotions, and that twice as many pleasant emotions were experienced during odor-evoked nostalgia than what had been previously found in a study examining music-evoked nostalgia [41].

Thus, as with the marked positivity of odor-evoked memories, feelings of nostalgia that are elicited by odors are more pleasant than nostalgic reminiscences elicited by other sensory stimuli.

It should be noted that odor-evoked memories can also elicit unpleasant emotions. Indeed they can be exceptionally potent triggers in post-traumatic stress disorder (PTSD). Case studies of PTSD have documented how odors that are associated with a traumatic event for a given individual (e.g., diesel, after-shave) evoke intense PTSD flashbacks which persist for decades, and do not extinguish with time [34].

Moreover, in a laboratory investigation of aversive memories it was found that among healthy college students who were asked to recall scenes from a traumatic documentary, which one week earlier had been paired with either an olfactory, visual or auditory cue, the olfactory cue led to more arousing, detailed and unpleasant memories of the documentary than the auditory cue did [33]. These findings caution that depending upon an individual’s past experience with an odor, the emotional states and responses that it elicits can be very negative.

Odor-Evoked Memory and Physiological Responses

Positive emotional states have generally been shown to improve physical health and longevity [43]. Therefore eliciting positive emotions through odor-evoked memory should have favorable health outcomes. Considerable empirical research has demonstrated that through odor-associative learning mechanisms—when via evaluative conditioning an odor takes on the meaning of an event to which it has been paired—odor perception and behavior in the presence of these odors can be reliably altered (see [44,45] for reviews).

Consistent with the principles of odor-associative learning [46], when an odor has become a proxy for the emotional properties of an event to which it is connected it can consequently produce downstream effects on physiology [47]. F

or example, an odor that evokes an exhilarating past personal episode can make one’s heart race and trigger a jolt of adrenalin—the physiological sequelae of the exhilarating emotional memory. Additionally, the direct connection between olfactory processing and the amygdala-hippocampal complex can make the emotions elicited by odor-evoked memories arise immediately upon perception.

Indeed, emotional primacy—when affect is elicited before a cognitive understanding of why the emotions produced has occurred—is another unique characteristic of odor-evoked memory [48].

Following the tenants of odor-associative learning, it has been experimentally demonstrated that odors that evoke positive emotional memories can have beneficial effects on physiological parameters of stress. In the study by Matsunaga et al. [36], pleasant odor-evoked autobiographical memories were also accompanied by a decrease in HR and an increase in SC, and these changes were correlated with self-reports of a happy mood and lower stress levels.

Correspondingly, the authors surmised that the positive emotions elicited by the odor-evoked memories were responsible for these positive physiological responses. Masaoka, Sugiyama, Katayama, Kashiwagi and Homma [35] further showed that when men and women ranging in age from 29 to 50 years were presented with a self-selected odor that evoked an autobiographical memory odor and two control fragrances, a pleasant odor (rose) and a neutral odor (chamomile) that did not elicit personally meaningful recollections, the autobiographical memory odor promoted deeper, slower and more relaxed breathing compared to odors that did not evoke a memory.

Slow, deep breathing is associated with relaxation and may stimulate whole-brain synchronization as it is seen in slow-wave sleep and meditation [49], both of which have neurological benefits. Masaoka et al. [35] therefore speculated that the respiratory changes that accompany the experience of pleasant odor-evoked memories may help lower stress and increase comfort—as feeling comfort was also reported by participants in this study.

Importantly, the evocativeness of the autobiographical memories triggered by odors and depth of breath were found to be greatest among individuals who scored high in trait anxiety, implying that the stress reducing benefits of odor-evoked memories may be strongest for those with the most need for it.

Chronic stress is correlated with a host of negative psychological and physiological consequences ranging from depression and memory-loss to stroke and cancer (for a few reviews see [50,51,52]).

A positive and calm mood is an antidote to stress, though when one is in a state of stress, pleasant moods are very hard to experience and maintain. Nevertheless, many people intuitively know that odors have the potential to elicit comfort. The act of “comfort smelling” where a person sniffs a garment worn by a loved one they are separated from has been demonstrated to conjure the feelings of love, support, and comfort representative of the absent person [53,54].

Following from the intuitive behavior of comfort smelling, the deliberate activation of comforting odor-evoked-memories by smelling an article of clothing, a fragrance, or any specific odor that for a given individual evokes soothing feelings of relaxation, may reduce stress.

Extrapolating from this I have further suggested that, when not in a state of physical hunger, merely smelling the aromas of “comfort foods”—foods which are especially sought after during times of difficulty as a function of their connection to memories of home, loved ones, and security—may be able to produce emotional succor and reduce stress without the negative consequences of over-eating [55].

Using odor-evoked memory to reduce stress can minimize the negative consequences that often accompany self-medicating methods such as excessive drug, alcohol and food intake, and may even be helpful in reducing cravings for various substances of abuse. Sayette and Parrot [38] found that smelling odors decreased the urge for cigarettes among chronic smokers, and odors that elicited autobiographical memories trended towards being most effective.

Several studies have now also reported that, at least in laboratory settings, odors can disrupt cravings for highly desirable calorie dense foods [56,57]. These studies on food craving did not assess whether the odors involved evoked personal memories. Nevertheless, it is likely that the mechanisms through which odors reduced food cravings were memory based.

For example, aromas connected to rich and filling foods could have elicited feelings of satiation, other odors may have triggered reminders of dieting intentions, and memories triggered by odors may have distracted individuals from their immediate cravings and thus disrupted capitulating to these urges [55]. These possibilities now need to be addressed in further research.

Neuroimaging studies investigating brain-immune interactions have revealed that prefrontal regions, such as the ventromedial prefrontal cortex (vmPFC) and the orbitofrontal cortex (OFC), regulate peripheral immune activities such as the proportion of natural killer cells among peripheral circulating lymphocytes [58,59]. Since the OFC is the secondary olfactory cortex it follows that odors may be able to exert a direct influence on immune responses.

Recent research that has examined physiological parameters associated with odor-evoked memory has found that odor-evoked memories may decrease systemic inflammation. Matsunaga et al. [36] demonstrated that pleasant odor-evoked memories were accompanied by a decrease in plasma levels of the inflammatory cytokine interleukin 2 (IL-2).

IL-2 is normally produced by T-lymphocytes during an immune response. A decrease in peripheral IL-2 therefore implies an inhibition of inflammation. As such, Matsunaga et al. [36] suggested that the positive feelings accompanying odor-evoked memories were able to decrease levels of peripherally circulating pro-inflammatory cytokines.

To further investigate the relationship between odor-evoked memory and brain-immune interactions, Matsunaga and colleagues [37] conducted an experiment where healthy men and women underwent positron emission tomography (PET) while they were exposed to a perfume that they had selected as eliciting an autobiographical memory and a pleasant unfamiliar perfume that did not have any personal significance for them (control fragrance) and plasma concentration of several inflammatory cytokines were measured.

Results showed that the self-selected odors elicited more positive emotions and autobiographical memories than the control odor, and importantly that levels of the peripheral proinflammatory cytokines, tumor necrosis factor-α (TNF-α) and interferon-γ (IFN-γ), were significantly reduced after experiencing an odor that evoked an autobiographical memory.

IL-2 was measured in this study but was not found to vary as a function of odor exposure condition, unlike Matsunaga group’s previous study [36].

The PET data further revealed that the medial orbitofrontal cortex (mOFC) and precuneus/posterior cingulate cortex (PCC) were significantly activated during experiences of odor-evoked autobiographic memory, and correlational analyses indicated that activation of the mOFC and precuneus/PCC were negatively associated with IFN-γ concentration.

Increased levels of proinflammatory cytokines, such as TNF-α and IFN-γ, can induce depressive symptoms [60]. Moreover, recent studies in psychoneuroimmunology have shown that emotional experiences can modulate the secretion of proinflammatory cytokines from immune cells, and that psychological stressors, such as anxiety, can promote secretion of proinflammatory cytokines [61].

It has also been demonstrated that happy feelings can suppress the secretion of proinflammatory cytokines and that they have favorable effects on health and wellbeing [62]. The results from Matsunaga’s group [37], therefore, suggest that a brain-immune interaction occurs during the experience of emotionally positive odor-evoked autobiographical memories such that the precuneus/PCC and mOFC, which regulate the secretion of peripheral proinflammatory cytokines, produces a decrease in peripheral pro-inflammatory responses.

Excessive inflammation has been implicated as the precursor to nearly every deleterious physical condition [63]. If odor-evoked-memories have the ability to reduce inflammation, even if the effects are minimal, it would be beneficial.

A caveat to over-reaching on this conclusion, however, is that blood tests in the Matsunaga experiments [36,37] were taken within two minutes of odor exposure so it is not known how long the positive effects from odor-evoked memory on immune function would last. Cautiously, one might posit that as long as a positive emotional state were maintained from an odor-evoked memory a reduction in inflammatory cytokines may persist.

Conversely, based on the extant research on stress and inflammation and studies demonstrating the link between olfaction and brain-immune interactions, odor-evoked memories that elicit substantial distress, such as which occur in PTSD, may have the potential to increase inflammation, though this has not yet been empirically assessed.


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Source: University of Geneva


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