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Smell of Fear … in Humans
Similar to the social transmission of fear in rodents, a small study of 14 participants tested how perturbing one's internal state through anxiety provocation would change the perception and associative responses of a neutral odorant.
The experiment used four neutral odorants (acetophenone, guaiacol, anisole, and eugenol) and two negative odorants (trimethylamine and valeric acid). Combinations of these scents were incorporated to form a neutral pure odor, a neutral odor mixture, and a negative smell. The experiment consisted of exposing the subjects to two neutral odor conditions and one negative smell condition. The negative phase was used as a filler and to prevent habituation to the neutral smells. Pure air served as the baseline and control. The authors measured results using functional magnetic resonance imaging (fMRI) techniques and olfactory interpretation and odor detection tasks. They further analyzed neural connectivity to determine the pathways involved in modulating this state-dependent process.
The results indicated that that after inducing an anxious state in volunteers, the previous smell of neutral odors became unpleasant and harder to detect than prior to when the participants were frightened.The authors also found that "anxiety amplified response to neutral odors in olfactory and emotion systems." Specifically, two regions of interest in the brain, the right olfactory OFC and right pregenual anterior cingulate gyrus (pgACC), were determined to be a strong main effect in how anxiety heightened responses to the neutral odors. Furthermore, the olfactory response to the smell created more anxiety "via strengthened (afferent or efferent) connections between amygdala and all levels of the olfactory cortical hierarchy."49 This study provided strong support that emotions and odors could be conditionally programmed and this could lead to changes in physiology and neurology in humans.
Odor, Emotions, the Amygdala, and Pain
It has been suggested that the neurobiological circuitry in emotional and physical pain is similar and in close proximity, such that somatic pain can continue, even when the physical healing process is completed.50 For example, there has been epidemiological evidence establishing a connection between the emotional impact of posttraumatic stress disorder (PTSD) and chronic pain.50-53
The connection between a history of psychological or emotionally charged events and painful conditions has also been implicated in many clinical studies.54-58 According to a 2009 article in Current Pain and Headache Reports:
The association of traumatic exposures with posttraumatic stress disorder (PTSD) and other mental health conditions is well known. Patients with chronic pain, particularly headache disorders and fibromyalgia (FM), associated with psychological traumas need a special management strategy. Diagnosis of headache disorders and FM in traumatized patients and collecting the clinical history of a traumatic event or diagnosing PTSD in chronic pain patients is of great importance. Psychotherapy and pharmacotherapeutic options should be started on patients with comorbid PTSD and headache disorders and/or FM.55
As suggested in rodents and mammals, olfactory stimuli can serve to modulate emotional expression and physiology. The following human studies also demonstrate this cued association with pain perception.
One small study of 16 male combat veterans, in which 8 were diagnosed with PTSD and 8 served as controls, sought to measure neural correlates of olfaction in PTSD. First, a baseline olfactory acuity assessment was performed. Then, all subjects were exposed to a set of four smells linked to affective responses as follows: diesel (related to traumatic memories of combat), odorless air (neutral odor), vanilla/coconut (positive scent), and hydrogen sulfide (H2S) (negative hedonic nontraumatic stimulus).
The researchers measured changes in responses to the smells by (1) assessing regional cerebral blood flow (rCBF), as determined by a positron emission tomographic (PET) imaging scan, and (2) assessment of psychophysiological and behavioral symptoms (i.e., the subjective distress, rating of pleasantness of the smell, emotional response ratings, PTSD symptoms, anxiety level, and dissociative symptoms) pre- and postinterventions. Salivary cortisol was also measured as an objective marker.
It was found that exposure to the diesel odorant was rated as unpleasant and distressing and was associated with increased symptomatology in the PTSD subjects significantly more than the control group. The H2S exposure caused the largest increase in PTSD symptoms, but not in the controls. According to the authors, "Both diesel and H2S caused intrusive memories and flashbacks in the PTSD group, whereas in the control group this was only the case in one patient, who reported a mild flashback with diesel."
The authors also noted a significant trend of an increase in diastolic blood pressure and heart rate with exposure to diesel in the PTSD subjects. PET imaging results indicated an increase in rCBF in the amygdala, insula, medial prefrontal cortex (mPFC), and anterior cingulate cortex (ACC) in the PTSD subjects. There was also decreased rCBF in lateral prefrontal cortex (lPFC) in comparison with combat controls. Furthermore, there were fewer rCBF changes on any smell in the PET imaging results of combat controls compared with the PTSD veterans. The controls also did not show amygdala activation upon diesel exposure.
The responses in brain patterns varied among subjects, most likely due to attributional differences. There was also no activity in the piriform cortex, which is usually considered among the primary olfactory cortex structures. The authors thought that this was related to the passive inhalation of the task versus recognition requirements and novel association processing.
Although there were some limitations (e.g., small sample size, the effect of familiarity with repeated exposures to similar smells, issues with standardization of intensity of smell, and the differential pathways of diesel and H2s igniting trigeminal activity), these could not account for the significant differences found, according to the authors.59 Their major finding of the amygdala activation with the diesel exposure was supportive of the associative emotional impact of odor, its connection to memories, and resultant physiological and neurological responses.
The above studies demonstrated an association between negatively emotionally charged states and resultant physiological responses, including pain perception, and cued olfactory stimuli. This has important implications for treatment of chronic pain conditions.
In the next section, I'll discuss the connection of olfaction to memories and physiological response patterns.
How Odor Affects Memory and Emotion
Many people have experienced that certain scents can conjure up specific emotional responses. As the rats' traumatic experiment with peppermint and the soldiers' response to the smell of diesel demonstrated, the environment and emotional state at the time of exposure to an odor can result in its association being pleasant or unpleasant. Consider how a whiff of a bakery's fresh batch of organic gluten-free cocoa-chip cookies can cause the fond remembrance of the warm conversations had in grandma's kitchen.
As noted with the small study of PTSD soldiers, odors may evoke memories that relate to these emotional responses. In fact, odor-evoked memory has been found to be vivid and specific, with the most familiar odors maybe evoking the greatest memory.60,61
This concept of odor-associated remembrances has been termed the Proust phenomenon. The term was coined in honor of the French writer Marcel Proust, for his romanticized description in his novel À la recherche du temps perdu of the memories evoked from the smell of a madeleine after soaking in tea.62,63
Although generally accepted as common sense (pun intended), not much research on this concept was done until recently. In 2012, one study provided preliminary support for Proust's namesake. The researchers subjected 70 female volunteers to a disturbing video while simultaneously spraying cassis (a representation of a unique odor), playing soft music, and displaying colorful lights on the wall.62,63 The video consisted of notable events, such as car crashes or news of genocide in Rwanda.
One week following the experiment, the researchers exposed the same subjects to either the cassis odor, the lights, or the music. They then requested that the participants think back about the film and rate their memory of it. When smelling the cassis odor or seeing the same colorful lights, the volunteers more vividly described the video. However, exposure to the music was comparable to not having any of the stimuli offered at all for recall. The study reported that an association between olfactory and visual stimuli connecting to emotional events was found; however, music seemed to be less provocative.62,63 The authors concluded, "Results revealed that odour-evoked memories of aversive events were more detailed, unpleasant and arousing than memories evoked by auditory, but not visual, triggers."63
Other studies have also reported that personal memories evoked by olfaction may be different from those relating to visual or acoustic information. It has been stated that memories for olfaction may form earlier in life than other senses and may be more powerful and explicit, and impact phenomenological qualities than other senses.60,61
It is interesting to note that the impact of music on memory has been studied with differing results, such in that positive emotions and high arousal levels have been associated with enhancement for recall of specific events.64,65 However, some authors suggest that the attractiveness of the event, versus the experienced arousal of the music, is what stimulates the autobiographical memory related to various melodies.64 This means that there may be a more complicated overlap between psychological response, memory, attention, imagery, and so on, and various brain networks in processing music versus odorants. These complexities, combined with the diverse stimuli, may have been a reason the auditory stimulus in the above experiment did not generate as strong an effect as smell and sight.
The Proust phenomenon not only seems to affect memory but also induces changes in physiology through these emotional memory experiences. This is for several biological reasons. As noted above, the amygdala is associated with smell and pain processing. During a stressful or aversive event, the amygdala is involved in the activation of the HPA neurohormonal and neurotransmitter pathways.66-68 This can result in physiological changes in white blood cell functioning, the inflammatory response, hormonal shifts, and many other organ and systematic effects.69-71 Due to the CRF receptors located within its structure, the amygdala may also act independently of the HPA stress response in regulating pain processing and inflammation.40-45 Therefore, the sense of smell, acting as a positive or negative stimulant, can have profound effects related to its connection to this emotional part of the brain.
In one study involving 23 healthy subjects (n = 5 males), researchers investigated how the smell of a personalized nostalgic odor changed mood states and autonomic nervous, endocrine, and immune activities. The authors measured the subjects' heart rate (HR), skin-conductance level (SCL), secretion of catecholamines (norepinephrine and epinephrine), and cytokines (i.e., interleukin-2 [IL-2], interleukin-4 [IL-4], interleukin 6 [IL-6], interleukin-10 [IL-10], and tumor necrosis factor-α [TNF-α]). The study sought to provide evidence that the sense of smell, as a powerful provocation of positive emotions, would evoke a change in these physiological functions.
First, the researchers had the subjects in the experimental "Proust condition" select an odor-associated nostalgic stimulus among various scents of perfume. A neutral smell, which was pretested and found not to evoke nostalgia, was used in control subjects. In order to assess for autobiographic memory of the odor and positive emotional valence, the participants evaluated the perceived intensity, arousal, pleasantness, and evocation of the memory by using the VAS (visual analog scale). At baseline, all measures, except for intensity, were significantly higher in the Proust subjects versus the controls.
The experiment consisted of a 10-min rest period in a chamber followed by baseline measurements and mood state rating. Mood was based on a seven-scale rating system: comfort, vigor, anxiety, fatigue, relaxation, irritation, and happiness. Following the baseline measures, participants were exposed to the control condition or the nostalgic odor for autobiographic memory induction (Proust condition) for 30 seconds. To prevent adaption, this was followed by rest for 30 seconds. The subjects next inhaled the odor again for another 30 seconds. After the second smelling condition, measurements were once again obtained.
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