Abstract
Background and Objectives
Visual auras in migraine have been extensively studied, but less is known about unusual experiences in other sensory domains, including whether they should be diagnostically considered as part of aura symptoms. This study aimed to examine the prevalence of multisensory aura experiences in migraine and their phenomenologic and clinical correlates.
Methods
Respondents were 729 participants with probable migraine, who completed an online study examining unusual sensory experiences. These comprised aura experiences in the auditory, visual, olfactory, somatic-tactile, and gustatory domains. Basic demographic and clinical information and migraine symptomatology were also collected. To facilitate groupwise comparisons, participants with probable migraine were divided into those with and without (visual) aura experiences.
Results
Endorsement of visual aura experiences was the highest (42.1%), whether in a single modality (44.2%) or multiple (55.8%) modalities, followed by somatic-tactile (32.0%), gustatory (21.9%), olfactory (18.6%), and auditory (11.0%) domains. Phenomenologic similarities, for instance, in frequency, personification, and controllability, existed across sensory domains. Somatic-tactile and gustatory auras conversely exhibited greater duration and negative emotional valence. Participants with probable migraine with visual aura tended to report significantly more severe migraine symptoms relative to those with nonvisual or no aura.
Discussion
Our findings provide preliminary indication that unusual olfactory, somatic-tactile, and gustatory experiences in migraine are common and could be clinically significant as aura symptoms. Increased clinician and patient awareness and effective management of these symptoms are essential for a holistic therapeutic approach to migraine.
Introduction
Migraine has been classified as the third most common global disorder, with an estimated worldwide prevalence of 15%.1 The socioeconomic and personal burden of migraine is significant in terms of productivity loss, health care expense, mental health, and familial impacts,2 yet migraine is often underdiagnosed or undertreated.3 Clinical diagnosis of migraine is based on the International Classification of Headache Disorders, Third Edition (ICHD-3) criteria and is broadly divided into migraine with or without aura.4 Up to 38% of those with migraine routinely experience aura symptoms.5 There has been a focus on visual auras,6 though similar perceptual experiences in other sensory domains have been reported.7,8 These auditory or olfactory auras do not officially feature in ICHD-3 diagnostic guidelines. According to the ICHD-3, aura is defined as “fully reversible visual, sensory, or other CNS symptoms that usually develop gradually and are usually followed by headache and other associated migraine symptoms.”4 This study thus aimed to conduct a large-scale empirical investigation of multisensory aura experiences in the context of migraine and related phenomenologic features and migraine correlates.
Visual aura symptoms predominate in up to 98% of cases with migraine with aura.9 Visual auras have been methodically studied10-12 and can involve complex visual imagery, such as human figures13 or unknown entities.14 Though typically transient, these experiences can endure15 and be disconcerting or anxiety provoking.13,14 Notably, those with migraine with visual aura have reported significantly more severe migraine symptoms, in terms of number of headache days per month, impact of migraine symptoms, and general pain levels, relative to those without.9
Auditory symptoms in migraine usually involve phonophobia, hearing loss, or tinnitus.5 Complex auditory-verbal experiences have also been noted, mostly in case reports.16-20 A retrospective case claimed that 58% of 12 patients heard voices; often lasting less than an hour (67%) and mostly concurrent with headache (75%).7 However, the small sample size and comorbid depression (67%) were major drawbacks limiting its generalizability.
Olfactory symptoms are similarly not uncommon; up to 96% of those with migraine allegedly experienced osmophobia, with 6% reporting olfactory experiences,21 where rotting,22 animal-like, burning,23 or specific food24 odors have been described. In a pair of small-scale empirical studies,8,25 the mean age of first olfactory aura ranged from 32 to 35 years, manifesting frequently in female participants with migraine (74%–82%), lasting 5–60 minutes (45%–84%), occurring before (64%–100%) or concurrent with (27%–36%) headache, and noted as mostly unpleasant (74%). Psychiatric comorbidities existed in a minority of those with migraine (36%), involving anxiety and depressive (but not psychotic) disorders.25
Unusual perceptual events in other sensory domains have also been observed.5 For example, gustatory or somatic distortions involving the head or neck feature in some migraine episodes, though comorbid affective syndromes existed in a proportion of those with migraine.26 Others described recurrent distortions of time relative to motion or speech.27 Much remains unknown about these experiences, and further investigations are warranted to elucidate their specific associations with migraine symptoms.
In this study, we focused on complex aura experiences in visual and nonvisual domains. Several proponents have called for inclusion of olfactory aura symptoms owing to their characteristic pattern of occurrence and remittance in line with migraine treatment.8,25,28,29 Yet much remains unknown about auditory, tactile, and gustatory events. Our study aimed to answer these research questions:
What was the prevalence of aura experiences across the 5 main sensory domains? For experiences in more than 1 sensory modality, what were the most common combinations of senses involved? We hypothesized that endorsement of visual aura would be the highest (Hypothesis 1a), whether in single modality or multiple sensory modalities (Hypothesis 1b). Relative frequencies of the other modalities were unknown.
What were the phenomenologic characteristics of aura experiences across auditory, visual, olfactory, tactile, and gustatory domains?
Did migraine symptoms differ significantly across those with and without (visual) aura experiences? We hypothesized that participants with probable migraine with visual aura would report significantly more severe migraine symptoms, in terms of number of headache days per month, impact of migraine symptoms, and pain levels, relative to those without aura experiences (Hypothesis 2). Whether the group with nonvisual aura would exhibit more or less severe migraine symptoms was examined.
We also sought to explore whether there would be significant associations between select migraine symptoms and emotional distress related to aura experiences. This latter facet was chosen because of its relevance to the mental well-being of those with migraine.
Methods
Standard Protocol Approvals, Registrations, and Patient Consents
This study was approved by the Swinburne University of Technology Human Research Ethics Committee (#0215573-6917), and procedures conformed to the Declaration of Helsinki.30 Respondents provided informed consent.
Participants and Procedure
Respondents were 866 individuals recruited from 3 primary sources—general community (n = 356) based on social media advertising, Prolific research platform (n = 333), and first-year psychological students (n = 177) enrolled in the Research Experience Program at Swinburne University of Technology. Eligibility criteria were as follows: (1) aged 18 years or older, ii) sufficient English language proficiency to respond meaningfully, and iii) availability of a laptop, tablet, or mobile device with internet connectivity. Participation involved an hour-long online survey through Qualtrics. Stringent data cleaning was undertaken, where respondents who: (1) did not endorse 1 or more migraine episodes over their lifetime (n = 89), (2) completed less than 10% of total survey (n = 45), or (3) had a comorbid diagnosis of a schizophrenia spectrum disorder (SSD; n = 3) were excluded. The final dataset comprised 729 individuals.
Materials
Basic sociodemographic and health information was collected. Participants were also asked whether they had a migraine diagnosis from a medical practitioner (e.g., general practitioner, neurologist).
Multisensory aura experiences were assessed using 5 modules of the Multimodal Hallucinations Schedule (MHS). Each module investigates aura experiences within a primary sensory domain—auditory, visual, olfactory, somatic-tactile, and gustatory, commencing with a screening question. Respondents who provide an affirmative response are asked to rate specific characteristics of their experiences (i.e., frequency, co-occurrence with headache, age at aura onset, relationship to past trauma, duration, intensity, complexity, location, conviction, interaction, personification, controllability, emotional valence, distress, and impact on functioning), with add-on items for auditory (i.e., compliance, voices commenting, and voices conversing) and olfactory (i.e., self-smells) modules. Respondents who answer no to the screening question are directed to the next module. Most questions are rated on 6-point Likert scales (0–5), with higher scores indicating increased symptom severity.
Migraine symptoms were evaluated using the Migraine Screening Questionnaire (MSQ),31 alongside select items from the Burden of Migraine measure (BURMIG),32 supplemented by added questions of interest (i.e., age at migraine onset, number of lifetime episodes, severity of headache, typical migraine pain severity, and specific triggers). The MSQ comprises 5 items asking about the presence of headache and accompanying symptoms rated dichotomously. We selected 4 items gauging functional impact of migraine (measured in mean days per month) from the 77-item BURMIG. Other questions elicited a range of response types, including numeric, dichotomous, and tick boxes, and a sliding scale (0–10) to rate pain intensity.33
Statistical Analysis
Data analysis was performed with IBM SPSS Statistics, v.27. Data were presented as mean values and standard deviations, percentages, or median descriptors, as appropriate. A breakdown of missing data showed a high completion rate, with 91.5% of participants responding to at least 91% of the survey (see eTable 1, links.lww.com/CPJ/A482). Preliminary analysis of demographic and clinical information characterized our participants with probable migraine. To answer our first 2 research questions, descriptive statistics were reported. To answer our third research question, groupwise comparisons were conducted. Respondents were divided into 3 subgroups: participants with probable migraine with no aura (NA; n = 201), those with visual only or visual plus aura in 1 or more sensory modalities (VA+; n = 264), and those with all other nonvisual aura (in a single modality or multiple modalities; NVA; n = 264). One-way analyses of variances (ANOVAs) were conducted for continuous variables, with Welch F reported for violations of homoscedasticity. For categorical variables, chi-squared tests for independence were applied. To answer our fourth research question, Spearman correlations, with Bonferroni adjustments (i.e., 0.05/5 = 0.01), were used. An alpha level of 0.05 was set for statistical significance (unless otherwise stated), with relevant effect sizes provided.34
Data Availability
Dataset is available on request by qualified researchers-scientists. Requests require a concept proposal describing the purpose of data access, appropriate ethical approval, and provision for data security. All data analysis scripts and result files are available for review.
Results
Demographic and Clinical Information
Demographic and clinical characterization is summarized in Table 1. For clinical information, 64.6% reported a migraine diagnosis given by a medical professional; the rest had suspected migraine that was self-diagnosed, other-diagnosed, or not officially diagnosed. A small percentage endorsed neurologic disorders, with epilepsy being the most common. Psychiatric comorbidities were prevalent, affecting approximately half the sample; generalized anxiety and depressive disorders were frequent. More than half of respondents were prescribed medications, mostly for migraine management.
Table 1.
Demographic and Clinical Information of Participants With Probable Migraine (n = 729)
| Mean ± standard deviation or percentage | |
| Demographics | |
| Age (y) | 31.0 ± 10.4 |
| Biological sex (%) | 28.0 Male, 71.2 Female, 0.8% Non-binary |
| Highest education (%) | 26.4 Primary/secondary, 22.2 TAFE/trade, 50.6 Tertiary |
| Employment status (%) | 14.5 Unemployed/retired, 28.3 Student, 56.9 Employed |
| Country of residence (%) | 57.9 Oceania, 21.8 Americas, 13.2 UK/Europe, Africa 3.4, Others 0.7 |
| Ethnicities (%) | 44.4 European, 39.8 Oceania, 12.8 Americas, 7.4 African, 6.6 Asian, 5.8 Others |
| Clinical | |
| aMigraine diagnosis (% yes) | |
| General practitioner | 38.7 |
| Neurologist or other medical specialist | 25.9 |
| Self (or family/friend) or undiagnosed | 35.4 |
| bComorbid neurologic disorders (% yes) | 15.6 |
| Epilepsy | 1.5 |
| Traumatic brain injury | 1.2 |
| Multiple sclerosis | 0.4 |
| Stroke | 0.4 |
| Others (e.g., fibromyalgia) | 6.9 |
| cComorbid mental health disorders (% yes) | 56.9 |
| Generalized anxiety disorder | 33.3 |
| Depressive disorder(s) | 32.0 |
| Social anxiety disorder | 12.3 |
| Posttraumatic stress disorder | 11.4 |
| Panic disorder | 9.5 |
| Eating disorder(s) | 6.4 |
| Others (e.g., specific phobias) | 12.1 |
| dPrescribed medications (% yes) | 54.7 |
| For migraine management (% yes) | 41.0 |
Where the cumulative percentages for each demographic and clinical variable add up to less than 100%, this reflects missing or incomplete responses. On the contrary, respondents could have endorsed multiple ethnicities and comorbid neurologic and/or mental health disorders (summed percentages may therefore exceed 100).
Migraine diagnosis given by a general practitioner, neurologist, or other medical specialist.
No comorbid Alzheimer disease, Huntington disease, or Parkinson disease or subarachnoid or intracranial hemorrhage conditions were identified for neurologic disorders.
Comorbid schizophrenia spectrum disorder(s) was an exclusion criterion for mental health disorders (n = 3); these respondents had been excluded from analyses.
Prescribed medications included neurologic, psychiatric, and other drugs to treat general health conditions (e.g., hypertension, pain management).
Prevalence and Combination of Aura Experiences Across the Sensory Modalities
Percentages of lifetime or current aura experiences are summarized in Table 2. Visual aura were most prominent (42.1%), followed by somatic-tactile (32.0%), gustatory (21.9%), olfactory (18.6%), and auditory (11.0%) modalities. A quarter of respondents were unsure, believing they may possibly have had these experiences, but rarely or not strongly (nb. conservatively allocated to the No aura subgroup in subsequent analyses). Owing to differences in recruitment source and whether formal diagnosis of migraine was endorsed, post hoc heterogeneity analyses showed that reported prevalence rates did somewhat vary according to these factors, but were less pronounced for nonvisual domains (see eTables 2 and 3, links.lww.com/CPJ/A482).
Table 2.
Endorsement of Aura Symptoms in the Context of Migraine Across Each of the 5 Primary Sensory Modalities
| Number, percentage of participants | |||||
| Auditory (n = 729) | Visual (n = 723) | Olfactory (n = 694) | Somatic-tactile (n = 687) | Gustatory (n = 680) | |
| No; never had these experiences | 467, 64.1 | 280, 38.7 | 417, 60.1 | 329, 47.9 | 384, 56.5 |
| Maybe; possibly had these experiences, but rarely or not strongly | 182, 25.0 | 139, 19.2 | 148, 21.3 | 138, 20.1 | 147, 21.6 |
| Yes, lifetime aura experiences | 64, 8.8 | 213, 29.5 | 99, 14.3 | 150, 21.8 | 126, 18.5 |
| Yes, current aura experiences (within past 2 wk) | 16, 2.2 | 91, 12.6 | 30, 4.3 | 70, 10.2 | 23, 3.4 |
Based on a conservative approach, only respondents who had endorsed Lifetime or Current aura experiences were counted toward Yes aura subgroups in subsequent analyses; those who had selected No or Maybe were allocated to the No aura subgroup.
Combinations of sensory modalities involved are summarized in Table 3. Aura in a single modality was most common, with endorsements diminishing as the number of sensory modalities increased. For unisensory aura, visual was most common, with the rest of the modalities following the same order in Table 2. Visual + somatic-tactile, visual + olfactory + somatic-tactile, and visual + olfactory + somatic-tactile + gustatory were the most prevalent combinations when 2, 3 or 4 modalities were considered, respectively. Auditory involvement in multisensory aura was largely absent, though a small fraction endorsed all 5 sensory modes.
Table 3.
Combination of Sensory Modalities Within Aura Endorsed by Participants With Probable Migraine (n = 680)
| Number, percentage of participants | |
| No aura experiences | 201, 29.6 |
| One sensory modality | 250, 36.8 |
| Auditory only | 10, 1.5 |
| Visual only | 110, 16.2 |
| Olfactory only | 27, 4.0 |
| Somatic-tactile only | 65, 9.6 |
| Gustatory only | 38, 5.6 |
| Two sensory modalities | 140, 20.6 |
| Auditory + visual | 8, 1.2 |
| Auditory + olfactory | 2, 0.3 |
| Auditory + somatic-tactile | 11, 1.6 |
| Auditory + gustatory | 4, 0.6 |
| Visual + olfactory | 12, 1.8 |
| Visual + somatic-tactile | 41, 6.0 |
| Visual + gustatory | 23, 3.4 |
| Olfactory + somatic-tactile | 12, 1.8 |
| Olfactory + gustatory | 11, 1.6 |
| Somatic-tactile + gustatory | 16, 2.4 |
| Three sensory modalities | 62, 9.1 |
| Auditory + visual + olfactory | 4, 0.6 |
| Auditory + visual + somatic-tactile | 8, 1.2 |
| Auditory + visual + gustatory | 3, 0.4 |
| Auditory + olfactory + somatic-tactile | 2, 0.3 |
| Auditory + olfactory + gustatory | 1, 0.1 |
| Auditory + somatic-tactile + gustatory | 4, 0.6 |
| Visual + olfactory + somatic-tactile | 14, 2.1 |
| Visual + olfactory + gustatory | 12, 1.8 |
| Visual + somatic-tactile + gustatory | 11, 1.6 |
| Olfactory + somatic-tactile + gustatory | 3, 0.4 |
| Four sensory modalities | 22, 3.2 |
| Auditory + visual + olfactory + somatic-tactile | 4, 0.6 |
| Auditory + visual + olfactory + gustatory | 1, 0.1 |
| Auditory + visual + somatic-tactile + gustatory | 4, 0.6 |
| Auditory + olfactory + somatic-tactile + gustatory | 1, 0.1 |
| Visual + olfactory + somatic-tactile + gustatory | 12, 1.8 |
| Five sensory modalities | 5, 0.7 |
Only respondents who completed all screening questions for each of the 5 sensory modalities were included in these analyses.
Phenomenologic Characteristics of Aura Experiences Across the Sensory Modalities
Descriptive phenomenology of aura across the 5 sensory modalities is summarized in Table 4 (nb. For a detailed breakdown by sensory modality, see eTables 4–8, links.lww.com/CPJ/A482). For all modalities, aura experiences took place at least once a month, before headache onset in the case of visual aura, but coinciding with headaches for the rest. Age at onset was similar in the early twenties, with some association with past trauma for the auditory domain, but less so for others. Auditory, visual, and olfactory aura lasted a few minutes per episode, but somatic-tactile and gustatory aura persisted for up to an hour. Most respondents reported visual, olfactory, and somatic-tactile aura as akin to corresponding real-life stimuli, but auditory and gustatory aura were less intense. Single words, simple forms, and itching/prickly were most likely for auditory, visual, and somatic-tactile aura respectively, with more complex sensations for olfactory and gustatory aura. Visual aura mostly occurred within the right visual field, whereas localization differed for the rest.
Table 4.
Phenomenology of Aura Symptoms Across Each of the 5 Primary Sensory Modalities in the Context of Migraine
| Median descriptor (or percentage or mean ± standard deviation) | |||||
| Auditory (n = 80) | Visual (n = 304) | Olfactory (n = 129) | Somatic-tactile (n = 220) | Gustatory (n = 149) | |
| Frequency | At least once a month | At least once a month | At least once a month | At least once a month | At least once a month |
| Co-occurrence with headache(s) | 38.8% During | 26.0% Before and during | 28.7% During | 31.4% During | 30.9% During |
| Age at aura onset (y) | 21.4 ± 9.7 | 19.4 ± 8.7 | 21.3 ± 8.6 | 20.0 ± 7.5 | 20.4 ± 8.4 |
| Trauma related (% yes) | 10.0 | 6.9 | 7.0 | 5.5 | 4.7 |
| Duration | Up to a few minutes | Up to a few minutes | Up to a few minutes | Ten minutes to an hour | Ten minutes to an hour |
| Intensity | Quiet, like a whisper | Same as regular image | Same as typical smells | Light to medium pressure | Intermittent taste |
| Complexity | Single words | Simple forms | Gas, petrol, smoke, or burning smells | Itching or prickling | Metallic |
| Location | Inside and outside head | Usually on right side | No specific location | Usually on or from body | Usually on tongue |
| Conviction | Possibly real, but unsure | Most likely not real | Possibly real, but unsure | Possibly real, but unsure | Probably real |
| Interaction | No interaction | No interaction | Only when intense | Sometimes | Only when intense |
| Compliance (auditory) | No commands | — | — | — | — |
| Personification | No personification | No personification | No personification | No personification | No personification |
| Controllability | No control | No control | No control | No control | No control |
| Emotional valence | Only neutral or positive | Only neutral or positive | Only neutral or positive | Rarely or occasionally negative | Some negative |
| Distress | Some discomfort | A little discomfort | A little discomfort | Some discomfort | A little discomfort |
| Impact on functioning | Interferes with few activities | Interferes with several activities | No impact | Interferes with several activities | No impact |
Conviction as to veracity was low for visual aura and high for gustatory aura, with mixed insight for the other modalities. Respondents were unlikely to react to auditory or visual aura and did so for olfactory (e.g., opening a window for better ventilation) and gustatory (e.g., chewing gum to get rid of taste) aura only when these were intense, but responded to somatic-tactile (e.g., rubbing affected area) aura frequently. For all modalities, there was no personification, but also no control in terms of the start, end, or content of aura. Neutral or positively valenced content was endorsed for auditory, visual, and olfactory aura, with occasional and some negative content for somatic-tactile and gustatory experiences, respectively. Visual, olfactory, and gustatory aura elicited little discomfort, with auditory and somatic-tactile experiences engendering more discomfort. Olfactory and gustatory aura had minimal impact on day-to-day function, auditory aura caused interference with a few daily activities, whereas visual and somatic-tactile aura interfered with several daily activities.
Comparisons of Migraine Symptoms in Those With and Without Visual Aura
Groupwise comparisons of demographic and clinical information and migraine symptoms between those with and without visual aura are summarized in Table 5. The VA+ group was significantly older than the NVA group, and the VA+ group had significantly more female participants and greater psychiatric comorbidity than the NA group. No other significant group differences were found.
Table 5.
Groupwise Comparisons of Demographic and Clinical Information and Migraine Symptoms for Participants With Probable Migraine With and Without (Visual) Aura
| Mean ± standard deviation or percentage | Statistics | ||||||
| NA (n = 201) | VA+ (n = 264) | NVA (n = 264) | F/χ2 | p Value | η2/V | Group contrasts | |
| Demographic and clinical information | |||||||
| Age (y) | 31.3 ± 11.1 | 32.4 ± 10.1 | 29.3 ± 10.0 | 5.8 | 0.003 | 0.016 | VA+>NVA |
| Biological sex (% female) | 62.0 | 83.3 | 66.7 | 30.5 | <0.001 | 0.145 | NA<VA+ |
| Comorbid neurologic disorders (% yes) | 12.5 | 18.9 | 14.9 | 3.7 | 0.153 | 0.072 | — |
| Comorbid mental health disorders (% yes) | 48.0 | 64.8 | 56.5 | 13.1 | 0.001 | 0.135 | NA<VA+ |
| Migraine symptoms | |||||||
| Age at migraine onset (y) | 18.0 ± 7.7 | 16.4 ± 6.9 | 17.7 ± 5.9 | 3.7b | 0.026 | 0.011 | NA>VA+ |
| Lifetime migraine episodes (% <5, 5–10, 11–19, 20+ episodes) | 21.3, 22.3, 11.7, 44.7 | 6.5, 13.0, 11.8, 68.7 | 18.0, 13.0, 11.8, 45.5 | 44.2 | <0.001 | 0.182 | <5 episodes: NA = NVA>VA+ 20+ episodes: NA = NVA<VA+ |
| aHeadache frequency (% yes) | 25.4 | 43.1 | 29.9 | 17.9 | <0.001 | 0.164 | NA<VA+ |
| Whether or not…(% yes) | |||||||
| Frequent and intense headaches | 77.9 | 86.3 | 80.1 | 5.9 | 0.053 | 0.095 | — |
| Headaches lasting >4h | 66.7 | 78.9 | 65.5 | 12.6 | 0.002 | 0.138 | NA = NVA<VA+ |
| Accompanied by nausea | 53.3 | 69.6 | 62.0 | 12.6 | 0.002 | 0.139 | NA<VA+ |
| Bothered by light or noise | 85.6 | 94.9 | 87.4 | 12.5 | 0.002 | 0.138 | NA = NVA<VA+ |
| Limited physical or intellectual activities | 87.1 | 91.8 | 85.0 | 5.6 | 0.061 | 0.092 | — |
| Mean days per month… | |||||||
| Experienced headaches | 4.7 ± 5.8 | 7.7 ± 8.5 | 5.5 ± 5.8 | 9.8b | <0.001 | 0.033 | NA = NVA<VA+ |
| Missed work or school | 1.9 ± 2.9 | 4.0 ± 6.4 | 2.7 ± 5.3 | 11.7b | <0.001 | 0.029 | NA = NVA<VA+ |
| Productivity reduced by half or more | 4.2 ± 5.4 | 5.9 ± 6.8 | 4.5 ± 5.6 | 4.6b | 0.011 | 0.015 | NA = NVA<VA+ |
| Missed family, social, or leisure activities | 2.3 ± 3.5 | 5.0 ± 7.0 | 3.2 ± 4.5 | 14.6b | <0.001 | 0.044 | NA = NVA<VA+ |
| Typical pain severity (0–10) | 6.6 ± 1.9 | 7.0 ± 2.0 | 6.7 ± 2.0 | 3.0 | 0.052 | 0.009 | — |
| Specific triggers identified (% no, unsure, yes) | 8.0, 7.0, 85.1 | 8.3, 7.2, 84.5 | 6.4, 24.6, 68.9 | 44.5 | <0.001 | 0.175 | Unsure: NA = VA+<NVA Yes: NA = VA+>NVA |
NA = No aura; VA+ = visual aura only or plus involvement of 1 or more other sensory modalities; NVA = all other nonvisual aura, whether unisensory or multisensory.
Headache frequency operationalized as experiencing migraine headaches on at least 8 days per month for more than 3 months.
Welch F.
The VA+ group reported significantly earlier age at migraine onset and greater headache frequency (see Table 5 footnotes for operationalization), more likely to be accompanied by nausea, than the NA group. The number of lifetime migraine episodes also differed, with the NA and NVA groups reporting significantly fewer episodes (<5), and the VA+ group reporting significantly more episodes (20+). A significantly greater proportion of the VA+ group reported headaches lasting more than 4 hours and being bothered by light or noise, relative to the other groups. The VA+ group also endorsed significantly more mean days per month lost to headaches, missing work or school, or leisure activities and reduced productivity by half or more, relative to the other groups. A significantly greater proportion of the NA and VA+ groups were able to identify specific migraine triggers, relative to the NVA group. No other significant group differences were found.
Correlations Between Select Migraine Symptoms and Emotional Distress Related to Aura
Headache frequency was not significantly correlated with aura-related emotional distress across any of the sensory modalities (r = 0.018–0.223-, p = 0.061–0.798, n = 71–269). Migraine impact on functioning was positively significantly associated with emotional distress related to auditory (r = 0.448, p < 0.001, n = 71), olfactory (r = 0.288, p = 0.002, n = 117), and somatic-tactile (r = 0.214, p = 0.002, n = 204), but not visual (r = 0.135, p = 0.029, n = 260) or gustatory (r = 0.173, p = 0.042, n = 138), aura.
Discussion
This study aimed to: (1) document the prevalence of multisensory aura experiences in migraine, (2) examine related phenomenologic characteristics, and (3) investigate whether participants with probable migraine endorsing visual aura reported significantly more severe migraine symptoms than those with aura in other sensory modalities or no aura.
Hypothesis 1a predicting that aura experiences in the visual domain would be endorsed with the highest frequency was supported. In order of current magnitude, this was followed by the somatic-tactile, gustatory, olfactory, and auditory modalities (Table 2). Hypothesis 1b predicting that endorsement of unisensory or multisensory visual aura would be the highest, regardless of whether 1 (16.2%), 2 (12.4%), 3 (7.7%), or 4 (3.1%) modalities were considered was also supported (Table 3). Our findings need to be contextualized in 2 ways. First, these percentages do not represent true prevalence as derived from large-scale epidemiologic studies. Indeed, our figures may be inflated; self-selection biases could be at play, where those with migraine with an interest in these unusual sensory events were overrepresented. Second, a converse consideration is that our elevated endorsement of multisensory aura (cf. reference 12) indicates many with migraine do have these experiences, which are routinely overlooked. For example, somatic-tactile aura were endorsed by almost a third of our sample, and yet this has received limited attention in migraine studies. This could be because targeted questions are not regularly asked in clinical and research assessments. That these symptoms are sometimes stigmatized and typically relegated to the psychiatric realm only exacerbates this issue. A proportion of respondents reporting they were unsure about having had these multisensory aura signified a lack of patient awareness as well.
Our second research question investigating phenomenologic characteristics of aura experiences across the 5 main sensory domains yielded notable findings. Multisensory aura mostly coincided with headaches for all sensory modalities (except visual, where it tended to precede). These temporal differences could reflect involvement of distinct neurologic networks,35 but perhaps also explained lesser consideration of nonvisual aura as migraine symptoms. Age at aura onset was similar across sensory modalities and comparable with that for visual aura (cf. references 10-12), but younger than noted for olfactory aura (cf. references 8,25). With minor exceptions, the somatic-tactile and gustatory domains stood out for remaining phenomenologic parameters examined. These had the longest durations, were associated with negative valence, and had the highest interaction and conviction levels, respectively, with somatic-tactile aura engendering the most emotional discomfort (alongside auditory aura) and greatest impact on functioning (alongside visual aura).
Hypothesis 2 predicting that participants with probable migraine with visual aura would report significantly more severe migraine symptoms, in terms of number of headache days per month and impact of migraine symptoms measured by number of days of missed work or school, missed family, social, or leisure activities, and reduced productivity by half or more, but not pain levels, relative to those without aura experiences, was partly supported. Lack of significant differences in pain levels could be attributed to varying operationalizations, with our study referring to migraine-related pain, whereas past research9 has employed general pain ratings. These significant differences extended to those experiencing nonvisual aura, which differed significantly from the visual aura, but not no aura, subgroups. Significant differences were also found in age at migraine onset, number of lifetime episodes, headache frequency, existence of long-lasting headaches, accompanied by nausea, and being bothered by light or noise, with the visual aura subgroup faring worse on all counts. This likely accounts for the unique focus on visual auras in migraine.
This study confers clinical implications worthy of further consideration. First, it is likely that olfactory and somatic-tactile, and possibly gustatory, auras are clinically significant, especially when considered from the perspectives of prevalence and distress. Even bearing psychiatric comorbidities in mind, prevalence figures for multisensory aura in our participants with probable migraine far exceed those typically endorsed within the general population (cf. 7% in reference 36) and point toward a possible role in migraine pathology. The only possible exception is auditory aura, which were within endorsement limits in the general population (cf. 5%–15% in reference 37). Yet significant positive associations were identified between emotional distress related to auditory, olfactory, and somatic-tactile aura and migraine impact on functioning. Pending further investigations, these symptoms likely merit diagnostic inclusion, whether within preexisting aura categories or as a new class of aura symptoms.
Second, seeking a thorough understanding of prevalence and phenomenology of aura symptoms across the sensory modalities will assist in early identification and treatment of migraine. This will include enhancing clinician and patient awareness of lesser-known aura modalities and combating stigma by normalizing symptoms typically associated with psychiatric illness. A lack of significant association between emotional distress related to visual aura and migraine impact on functioning likely underscores how recognition of visual auras may have somewhat alleviated its impact. Doing the same for nonvisual symptoms should bring similar benefits. Providing psychoeducation and management strategies for aura symptoms that cause distress or interfere with daily functioning should form part of holistic, effective migraine intervention.
This study was subject to some limitations. First, online administration meant that migraine diagnosis and aura experiences relied on self-report. Most of the respondents did receive a clinical diagnosis by a medical practitioner (64.6%). Yet our post hoc heterogeneity analyses revealed that our prevalence findings did somewhat vary as a function of whether a formal migraine diagnosis was endorsed (and specific recruitment source). These represent study limitations that need to be addressed through robust replication. However, collecting accurate information on aura can be tricky, partly owing to lack of awareness or understanding of such phenomena. Yet those with migraine also represent an appropriate cohort for online data collection, owing to largely intact insight. This methodology also allowed candid responses to a potentially sensitive topic and robust respondent numbers, amidst the COVID-19 pandemic.
Second, some significant demographic and clinical differences were observed that may have limited conclusions being drawn. Elevated psychiatric comorbidities in the visual aura subgroup was a potential issue, given unusual sensory experiences can be prominent in some psychiatric disorders. We did exclude few respondents with a schizophrenia spectrum disorder (n = 3), while remaining psychiatric diagnoses comprised high-prevalence anxiety and depressive disorders (Table 1). A certain level of psychiatric comorbidity, however, rendered our sample more representative of a typical migraine cohort. Third, the array of medications endorsed and potential drug interactions precluded a more nuanced analysis of possible medication effects. On the contrary, our study represents a comprehensive, large-scale foray into multisensory aura experiences in migraine, helping to shed much needed light on these clinically significant phenomena.
Several avenues for future research are evident. Robust face-to-face replication is the next logical step, such that a combination of semistructured and open-response questions posed by trained interviewers will facilitate the disentangling of true aura from other unusual sensory phenomena. There should be added focus on olfactory aura, where a case for diagnostic inclusion has already been made.8,25,28,29 Our findings implicating the phenomenologic significance of somatic-tactile and gustatory aura means these 2 domains are also deserving of attention. Enquiries into gustatory experiences in migraine may be fruitful, given its interplay with olfaction amid scant existing research.38 Upcoming studies into concurrent multisensory aura, where, for instance, a migraineur may simultaneously smell a burning odor and taste an acrid flavor could prove notable because this is the direction that broader hallucinations studies are taking.39,40
As part of comprehensive phenomenologic enquiry, future research can tap into basic sensory processing and relevant neurobiological correlates. It would be worthwhile to examine whether olfactory41 or gustatory42 abilities are impaired, and whether these potential deficits only transpire during a migraine episode with aura, or are enduring. Preliminary neuroimaging research has identified significantly enhanced functional connectivity between gustatory (and auditory) network(s) with primary and secondary visual cortices but failed to demonstrate similar aberrant activity within the olfactory cortex.35 Other specific migraine subgroups are worth extending the abovementioned enquiries to include women and children, both of whom are known to be more prone to unusual sensory experiences.43,44 In fact, the study of auditory45 and olfactory46 aura in children with migraine is already underway and should yield notable findings.
TAKE-HOME POINTS
→ Multisensory aura experiences (beyond the visual) are relatively prevalent in migraine.
→ Somatic-tactile and gustatory symptoms require further clinical and research attention.
→ These could be clinically significant as aura symptoms and require increased clinician-patient awareness.
→ Inclusive management of these multisensory aura symptoms is key to holistic migraine intervention.
To date, visual symptoms, including complex imagery, have been well-studied and officially recognized as prominent aura symptoms. Our preliminary findings have demonstrated that aura in olfactory, somatic-tactile, or even gustatory domains could be symptoms of clinical significance in migraine. When directly asked, candid accounts involving heightened prevalence and rich phenomenologic detail emerged. This signifies that further consideration of these migraine-related symptoms is essential for holistic and successful illness management moving forward.
Acknowledgment
The authors thank all respondents for their time and effort in completing this study.
Appendix. Authors
| Name | Location | Contribution |
| Wei Lin Toh, MPsych/PhD (Clinical) | Centre for Mental Health & Brain Sciences, Swinburne University of Technology, Melbourne, Victoria, Australia | Drafting/revision of the article for content, including medical writing for content; major role in the acquisition of data; study concept or design; and analysis or interpretation of data |
| Caitlin O. Yolland, PhD | Centre for Mental Health & Brain Sciences, Swinburne University of Technology, Melbourne, Victoria, Australia | Major role in the acquisition of data |
| Yixuan Li, BA | Centre for Mental Health & Brain Sciences, Swinburne University of Technology, Melbourne, Victoria, Australia | Major role in the acquisition of data |
| Iris E. Sommer, PhD | University Medical Center Groningen, University of Groningen, The Netherlands | Drafting/revision of the article for content, including medical writing for content |
| Susan Rossell, PhD | Centre for Mental Health & Brain Sciences, Swinburne University of Technology, Melbourne, Victoria, Australia | Drafting/revision of the article for content, including medical writing for content |
Study Funding
The authors report no targeted funding.
Disclosure
W.L. Toh is supported by a National Health and Medical Research Council (NHMRC) New Investigator project grant (GNT1161609), and S.L. Rossell is supported by a NHMRC Fellowship (GNT1154651). All other authors report no disclosures relevant to the manuscript. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/cp.
References
- 1.Steiner TJ, Stovner LJ, Birbeck GL. Migraine: the seventh disabler. Cephalalgia. 2013;33(5):289-290. doi: 10.1177/0333102412473843 [DOI] [PubMed] [Google Scholar]
- 2.World Health Organisation. Lifting the Burden: Atlas of Headache Disorders and Resources in the World 2011. World Health Organisation; 2011. [Google Scholar]
- 3.Pavone E, Banfi R, Vaiani M, Panconesi A. Patterns of triptans use: a study based on the records of a community pharmaceutical department. Cephalalgia. 2007;27(9):1000-1004. doi: 10.1111/j.1468-2982.2007.01401.x [DOI] [PubMed] [Google Scholar]
- 4.Headache Classification Committee of the International Headache Society. The International Classification of headache disorders, 3rd edition. Cephalalgia. 2018;38(1):1-211. [DOI] [PubMed] [Google Scholar]
- 5.Kelman L. The aura: a tertiary care study of 952 migraine patients. Cephalalgia. 2004;24(9):728-734. doi: 10.1111/j.1468-2982.2004.00748.x [DOI] [PubMed] [Google Scholar]
- 6.Schott GD. Exploring the visual hallucinations of migraine aura: the tacit contribution of illustration. Brain. 2007;130(6):1690-1703. doi: 10.1093/brain/aw1348 [DOI] [PubMed] [Google Scholar]
- 7.Miller EE, Grosberg BM, Crystal SC, Robbins MS. Auditory hallucinations associated with migraine: case series and literature review. Cephalalgia. 2015;35(10):923-930. doi: 10.1177/0333102414563088 [DOI] [PubMed] [Google Scholar]
- 8.Mainardi F, Rapoport A, Zanchin G, Maggioni F. Scent of aura? Clinical features of olfactory hallucinations during a migraine attack (OHM). Cephalalgia. 2017;37(2):154-160. doi: 10.1177/0333102416630580 [DOI] [PubMed] [Google Scholar]
- 9.Kim KM, Kim BK, Lee W, Hwang H, Heo K, Chu MK. Prevalence and impact of visual aura in migraine and probable migraine: a population study. Sci Rep. 2022;12(1):426. doi: 10.1038/s41598-021-04250-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Queiroz LP, Friedman DI, Rapoport AM, Purdy RA. Characteristics of migraine visual aura in Southern Brazil and Northern USA. Cephalalgia. 2011;31(16):1652-1658. doi: 10.1177/0333102411430263 [DOI] [PubMed] [Google Scholar]
- 11.Queiroz LP, Rapoport AM, Weeks RE, Sheftell FD, Siegel SE, Baskin SM. Characteristics of migraine visual aura. Headache. 1997;37(3):137-141. doi: 10.1046/j.1526-4610.1997.3703137.x [DOI] [PubMed] [Google Scholar]
- 12.Viana M, Tronvik EA, Do TP, Zecca C, Hougaard A. Clinical features of visual migraine aura: a systematic review. J Headache Pain. 2019;20(1):64. doi: 10.1186/s10194-019-1008-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Akiyama O, Kondo A, Akiyama I. Paediatric migraine with visual hallucination auras appearing in the form of a human body. BMJ Case Rep. 2019;2(12):12. doi: 10.1136/bcr-2019-232358 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.George D, Bernard P. Complex hallucinations and panic attacks in a 13-year-old with migraines: the alice in wonderland syndrome. Innov Clin Neurosci. 2013;10(1):30-32. [PMC free article] [PubMed] [Google Scholar]
- 15.Evans RW, Aurora SK. Migraine with persistent visual aura. Headache. 2012;52(3):494-501. doi: 10.1111/j.1526-4610.2012.02103.x [DOI] [PubMed] [Google Scholar]
- 16.Lo YL, Hameed S, Rumpel H, Chan LL. Auditory hallucinations and migraine of possible brainstem origin. J Headache Pain. 2011;12(5):573-575. doi: 10.1007/s10194-011-0355-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.van der Feltz-Cornelis CM, Biemans H, Timmer J. Hearing voices: does it give your patient a headache? A case of auditory hallucinations as acoustic aura in migraine. Neuropsychiatr Dis Treat. 2012;8:105-111. doi: 10.2147/NDT.S29300 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Vreeburg SA, Leijten FSS, Sommer IEC. Auditory hallucinations preceding migraine, differentiation with epileptic origin: a case report. Schizophr Res. 2016;172(1-3):222-223. doi: 10.1016/j.schres.2016.02.008 [DOI] [PubMed] [Google Scholar]
- 19.Grosberg BM, Tsang AY, Solomon S, Lipton RB. Migraine headache and auditory hallucinations. Headache. 2007;47(5):802-803. [Google Scholar]
- 20.Tarshish S, Robbins MS, Grosberg BM. Auditory hallucinations in adults with migraine. Neurology. 2009;72(11):A251. [Google Scholar]
- 21.Fornazieri MA, Neto AR, de Rezende Pinna F, et al. Olfactory symptoms reported by migraineurs with and without auras. Headache. 2016;56(10):1608-1616. doi: 10.1111/head.12973 [DOI] [PubMed] [Google Scholar]
- 22.Wolberg FL, Ziegler DK. Olfactory hallucination in migraine. Arch Neurol. 1982;39(6):382. [DOI] [PubMed] [Google Scholar]
- 23.Jion YI, Grosberg BM, Evans RW. Phantosmia and migraine with and without headache. Headache. 2016;56(9):1494-1502. doi: 10.1111/head.12890 [DOI] [PubMed] [Google Scholar]
- 24.Daniel C, Donnet A. Migrainous complex hallucinations in a 17-year-old adolescent. Headache. 2011;51(6):999-1001. doi: 10.1111/j.1526-4610.2010.01823.x [DOI] [PubMed] [Google Scholar]
- 25.Coleman ER, Grosberg BM, Robbins MS. Olfactory hallucinations in primary headache disorders: case series and literature review. Cephalalgia. 2011;31(14):1477-1489. doi: 10.1177/0333102411423315 [DOI] [PubMed] [Google Scholar]
- 26.Morrison DP. Abnormal perceptual experiences in migraine. Cephalalgia. 1990;10(6):273-277. doi: 10.1046/j.1468-2982.1990.1006273.x [DOI] [PubMed] [Google Scholar]
- 27.Dooley J, Gordon K, Camfield P. The rushes—a migraine variant with hallucinations of time. Clin Pediatr (Phila). 1990;29(9):536-538. doi: 10.1177/000992289002900912 [DOI] [PubMed] [Google Scholar]
- 28.Tiriticco M, Vanotti A, Mantica D, Coppola A. Migraine with exclusive olfactory aura: case report and literature review. Headache. 2020;60(10):2544-2547. doi: 10.1111/head.14014 [DOI] [PubMed] [Google Scholar]
- 29.Donat J, Donat T. Homeless in the world of the ICHD: migraine with olfactory aura. Headache. 2008;48(9):1383. doi: 10.1111/j.1526-4610.2008.01248.x [DOI] [PubMed] [Google Scholar]
- 30.World Medical Association. Declaration of Helsinki: ethical principles for medical research involving human subjects. Accessed September 14, 2017. wma.net. [PubMed]
- 31.Lainez MJ, Dominguez M, Rejas J, et al. Development and validation of the migraine screen questionnaire (MSQ). Headache. 2005;45(10):1328-1338. doi: 10.1111/j.1526-4610.2005.00265.x [DOI] [PubMed] [Google Scholar]
- 32.Andree C, Vaillant M, Rott C, Katsarava Z, Sandor PS. Development of a self-reporting questionnaire, BURMIG, to evaluate the burden of migraine. J Headache Pain. 2008;9(5):309-315. doi: 10.1007/s10194-008-0059-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Boonstra AM, Stewart RE, Koke AJ, et al. Cut-off points for mild, moderate, and severe pain on the numeric rating scale for pain in patients with chronic musculoskeletal pain: variability and influence of sex and catastrophising. Front Psychol. 2016;7:1466. doi: 10.3389/fpsyg.2016.01466 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Field A. Discovering statistics using SPSS, 3rd ed. Introducing Statistical Methods. Sage Publications; 2009. [Google Scholar]
- 35.Meylakh N, Henderson LA. Exploring alterations in sensory pathways in migraine. J Headache Pain. 2022;23(1):5. doi: 10.1186/s10194-021-01371-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Laloyaux J, Bless JJ, Hugdahl K, et al. Multimodal hallucinations are associated with poor mental health and negatively impact auditory hallucinations in the general population: results from an epidemiological study. Schizophr Res. 2019;210:319-322. doi: 10.1016/j.schres.2019.06.005 [DOI] [PubMed] [Google Scholar]
- 37.Toh WL, Moseley P, Fernyhough C. Hearing voices as a feature of typical and psychopathological experience. Nat Rev Psychol. 2022;1:72-86. [Google Scholar]
- 38.Finger TE, Silver WL. Neurobiology of Taste and Smell. Krieger Publishing; 1991. [Google Scholar]
- 39.Laroi F, Bless JJ, Laloyaux J, et al. An epidemiological study on the prevalence of hallucinations in a general-population sample: effects of age and sensory modality. Psychiatry Res. 2019;272:707-714. doi: 10.1016/j.psychres.2019.01.003 [DOI] [PubMed] [Google Scholar]
- 40.Toh WL, Bere M, Rossell SL. Distinguishing multimodal versus multisensory hallucinations in psychosis: key definitions and a way forward. Aust N Z J Psychiatry 2022;56(5):445-450. doi: 10.1177/00048674211031455 [DOI] [PubMed] [Google Scholar]
- 41.Rumeau C, Nguyen DT, Jankowski R. How to assess olfactory performance with the Sniffin' Sticks test. Eur Ann Otorhinolaryngol Head Neck Dis. 2016;133(3):203-206. doi: 10.1016/j.anorl.2015.08.004 [DOI] [PubMed] [Google Scholar]
- 42.Landis BN, Welge-Luessen A, Bramerson A, et al. "Taste strips": a rapid, lateralised, gustatory bedside identification test based on impregnated filter papers. J Neurol. 2009;256(2):242-248. doi: 10.1007/s00415-009-0088-y [DOI] [PubMed] [Google Scholar]
- 43.Morokuma Y, Endo K, Nishida A, et al. Sex differences in auditory verbal hallucinations in early, middle and late adolescence: results from a survey of 17 451 Japanese students aged 12-18 years. BMJ Open. 2017;7(5):e015239. doi: 10.1136/bmjopen-2016-015239 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Maijer K, Begemann MJH, Palmen S, Leucht S, Sommer IEC. Auditory hallucinations across the lifespan: a systematic review and meta-analysis. Psychol Med. 2018;48(6):879-888. doi: 10.1017/S0033291717002367 [DOI] [PubMed] [Google Scholar]
- 45.Rubin D, McAbee GN, Feldman-Winter LB. Auditory hallucinations associated with migraine. Headache. 2002;42(7):646-648. doi: 10.1046/j.1526-4610.2002.02153.x [DOI] [PubMed] [Google Scholar]
- 46.Ahmed MAS, Donaldson S, Akor F, Cahill D, Akilani R. Olfactory hallucination in childhood primary headaches: case series. Cephalalgia. 2015;35(3):234-239. doi: 10.1177/0333102414535998 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Dataset is available on request by qualified researchers-scientists. Requests require a concept proposal describing the purpose of data access, appropriate ethical approval, and provision for data security. All data analysis scripts and result files are available for review.