Download PDF
CC BY-NC-ND 4.0 · Int Arch Otorhinolaryngol 2021; 25(03): e355-e364
DOI: 10.1055/s-0040-1716572
Original Research

Cerebral Responses to Stationary Emotional Stimuli Measured by fMRI in Women with Persistent Postural-Perceptual Dizziness

Eliane Maria Dias von Söhsten Lins 
1   Department of Otorhinolaryngology, Hospital das Clínicas, Universidade de São Paulo, São Paulo, SP, Brazil
,
Roseli Saraiva Moreira Bittar 
1   Department of Otorhinolaryngology, Hospital das Clínicas, Universidade de São Paulo, São Paulo, SP, Brazil
,
Paulo Rodrigo Bazán 
2   Department of Radiology, Hospital das Clínicas, Universidade de São Paulo, São Paulo, SP, Brazil
,
Edson Amaro Júnior 
2   Department of Radiology, Hospital das Clínicas, Universidade de São Paulo, São Paulo, SP, Brazil
,
Jeffrey Paul Staab 
3   Department of Psychiatry, Mayo Clinic, Rochester, USA
› Author Affiliations Funding Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant/Award Number: '11/51266-5′)
› Further Information
Also available at
   Permissions and Reprints

Abstract

Introduction Persistent postural-perceptual dizziness (PPPD) is a functional vestibular disorder characterized by chronic dizziness, unsteadiness, and hypersensitivity to motion. Preexisting anxiety disorders and neurotic personality traits confer vulnerability to PPPD. High anxiety during acute vertigo or dizziness incites it. A functional magnetic resonance imaging (fMRI) study of chronic subjective dizziness found unexpectedly hypoactive responses to vestibular stimulation in cortical regions that integrate threat assessment and spatial perception.

Objective This fMRI study used non-moving, but emotionally charged visual stimuli to investigate the brain's activity of PPPD patients and control subjects.

Methods The participants included 16 women with PPPD and 16 age-matched women who recovered completely from acute episodes of vertigo or dizziness capable of triggering PPPD. Brain responses to positive, neutral, and negative figures from the International Affective Picture System were measured with fMRI and compared between the groups. Dizziness handicap, anxiety, and depression were assessed with validated questionnaires.

Results Between group analyses: Participants with PPPD showed reduced activity in anterior cingulate cortex and increased activity in left angular gyrus in response to negative versus positive stimuli, which was not observed in recovered individuals. Within group analyses: Participants with PPPD had increased activity in visuospatial areas (parahippocampal gyrus, intraparietal sulcus) in negative versus positive and negative versus neutral contrasts, whereas recovered individuals had increased activity in anxiety regions (amygdala, orbitofrontal cortex).

Conclusion Patients with PPPD may be more attuned to spatial elements than to the content of emotionally charged visual stimuli.

Keywords

anxiety - angular gyrus - anterior cingulate cortex - chronic dizziness - functional magnetic resonance imaging - persistent postural perceptual dizziness


Publication History

Received: 03 April 2020

Accepted: 23 July 2020

Article published online:
24 September 2020

© 2020. Fundação Otorrinolaringologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil

 

  • References

  • 1 World Health Organization. Persistent postural-perceptual dizziness. International Classification of Diseases, ICD-11 Beta Draft (Joint Linearization for Mortality and Morbidity Statistics), Accessed 30 September 2019. at https://icd.who.int/browse11/lm/en#/http://id.who.int/icd/entity/2005792829
  • 2 Staab JP, Eckhardt-Henn A, Horii A. et al. Diagnostic criteria for persistent postural-perceptual dizziness (PPPD): Consensus document of the committee for the Classification of Vestibular Disorders of the Bárány Society. J Vestib Res 2017; 27 (04) 191-208 DOI: 10.3233/VES-170622.
    CrossrefPubMedGoogle Scholar
  • 3 Dieterich M, Staab JP. Functional dizziness: from phobic postural vertigo and chronic subjective dizziness to persistent postural-perceptual dizziness. Curr Opin Neurol 2017; 30 (01) 107-113 DOI: 10.1097/WCO.0000000000000417.
    CrossrefPubMedGoogle Scholar
  • 4 Brandt T, Dieterich M. Phobischer Attacken-Schwankschwindel, ein neues Syndom. Munch Med Wochenschr 1986; 128: 247-250
    Google Scholar
  • 5 Jacob RG, Lilienfeld SO, Furman JMR, Durrant JD, Turner SM. Panic disorder with vestibular dysfunction: Further clinical observation and description of space and motion phobic stimuli. J Anxiety Disord 1989; 3: 117-130
    CrossrefGoogle Scholar
  • 6 Bronstein AM. Visual vertigo syndrome: clinical and posturography findings. J Neurol Neurosurg Psychiatry 1995; 59 (05) 472-476
    CrossrefPubMedGoogle Scholar
  • 7 Staab JP, Ruckenstein MJ. Expanding the differential diagnosis of chronic dizziness. Arch Otolaryngol Head Neck Surg 2007; 133 (02) 170-176
    CrossrefPubMedGoogle Scholar
  • 8 Staab JP. Chronic subjective dizziness. Continuum (Minneap Minn) 2012; 18 (5 Neuro-otology): 1118-1141
    Google Scholar
  • 9 Schniepp R, Wuehr M, Huth S, Pradhan C, Brandt T, Jahn K. Gait characteristics of patients with phobic postural vertigo: effects of fear of falling, attention, and visual input. J Neurol 2014; 261 (04) 738-746
    CrossrefPubMedGoogle Scholar
  • 10 Cousins S, Cutfield NJ, Kaski D. et al. Visual dependency and dizziness after vestibular neuritis. PLoS One 2014; 9 (09) e105426
    CrossrefPubMedGoogle Scholar
  • 11 Staab JP, Rohe DE, Eggers SD, Shepard NT. Anxious, introverted personality traits in patients with chronic subjective dizziness. J Psychosom Res 2014; 76 (01) 80-83
    CrossrefPubMedGoogle Scholar
  • 12 Chiarella G, Petrolo C, Riccelli R. et al. Chronic subjective dizziness: Analysis of underlying personality factors. J Vestib Res 2016; 26 (04) 403-408
    CrossrefPubMedGoogle Scholar
  • 13 Yan Z, Cui L, Yu T, Liang H, Wang Y, Chen C. Analysis of the characteristics of persistent postural-perceptual dizziness: A clinical-based study in China. Int J Audiol 2017; 56 (01) 33-37
    CrossrefPubMedGoogle Scholar
  • 14 Staab JP, Ruckenstein MJ. Which comes first? Psychogenic dizziness versus otogenic anxiety. Laryngoscope 2003; 113 (10) 1714-1718
    CrossrefPubMedGoogle Scholar
  • 15 Tschan R, Best C, Beutel ME. et al. Patients' psychological well-being and resilient coping protect from secondary somatoform vertigo and dizziness (SVD) 1 year after vestibular disease. J Neurol 2011; 258 (01) 104-112
    CrossrefPubMedGoogle Scholar
  • 16 Godemann F, Siefert K, Hantschke-Brüggemann M, Neu P, Seidl R, Ströhle A. What accounts for vertigo one year after neuritis vestibularis - anxiety or a dysfunctional vestibular organ?. J Psychiatr Res 2005; 39 (05) 529-534
    CrossrefPubMedGoogle Scholar
  • 17 Heinrichs N, Edler C, Eskens S, Mielczarek MM, Moschner C. Predicting continued dizziness after an acute peripheral vestibular disorder. Psychosom Med 2007; 69 (07) 700-707
    CrossrefPubMedGoogle Scholar
  • 18 Indovina I, Riccelli R, Staab JP, Lacquaniti F, Passamonti L. Personality traits modulate subcortical and cortical vestibular and anxiety responses to sound-evoked otolithic receptor stimulation. J Psychosom Res 2014; 77 (05) 391-400
    CrossrefPubMedGoogle Scholar
  • 19 Riccelli R, Indovina I, Staab JP. et al. Neuroticism modulates brain visuo-vestibular and anxiety systems during a virtual rollercoaster task. Hum Brain Mapp 2017; 38 (02) 715-726 DOI: 10.1002/hbm.23411.
    CrossrefPubMedGoogle Scholar
  • 20 Indovina I, Riccelli R, Chiarella G. et al. Role of the insula and vestibular system in patients with chronic subjective dizziness: An fMRI study using sound-evoked vestibular stimulation. Front Behav Neurosci 2015; 9: 334
    CrossrefPubMedGoogle Scholar
  • 21 Wurthmann FS, Nägel S, Holle D. et al. Gray matter decrease in phobic postural vertigo–a VBM study. Klin Neurophysiol 2012; 43: 119
    Article in Thieme ConnectGoogle Scholar
  • 22 Costa PT, McCrae RR. NEO Personality Inventory Revised (NEO-PI-R™). Lutz, FL, USA: Psychological Assessments Resources, Inc.; 1992
    Google Scholar
  • 23 Lang PJ, Bradley MM, Cuthbert BN. International Affective Picture System (IAPS): Technical Manual and Affective Ratings. http://csea.phhp.ufl.edu/media.html
  • 24 Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983; 67 (06) 361-370
    CrossrefPubMedGoogle Scholar
  • 25 Spielberger CD. State-Trait Anxiety Inventory: Bibliography (2nd ed.).. Palo Alto, CA: Consulting Psychologists Press; 1989
    Google Scholar
  • 26 Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation; 1996
    Google Scholar
  • 27 Jacobson GP, Newman CW. The development of the Dizziness Handicap Inventory. Arch Otolaryngol Head Neck Surg 1990; 116 (04) 424-427
    CrossrefPubMedGoogle Scholar
  • 28 Bittar RS, Lins EM. Clinical characteristics of patients with persistent postural-perceptual dizziness. Rev Bras Otorrinolaringol (Engl Ed) 2015; 81 (03) 276-282
    CrossrefPubMedGoogle Scholar
  • 29 Bittar RSM, Bottino MA, Simoceli L. et al. Vestibular Impairment secondary to glucose metabolic disorders: reality or myth?. Rev Bras Otorrinolaringol (Engl Ed) 2004; 70: 800-805
    CrossrefGoogle Scholar
  • 30 Bittar RSM, Santos MD, Mezzalira R. Glucose metabolism disorders and vestibular manifestations: evaluation through computerized dynamic posturography. Rev Bras Otorrinolaringol (Engl Ed) 2016; 82 (04) 372-376
    Google Scholar
  • 31 Thompson KJ, Goetting JC, Staab JP, Shepard NT. Retrospective review and telephone follow-up to evaluate a physical therapy protocol for treating persistent postural-perceptual dizziness: A pilot study. J Vestib Res 2015; 25 (02) 97-103 , quiz 103–104
    PubMedGoogle Scholar
  • 32 Mari JJ, Williams P. A validity study of a psychiatric screening questionnaire (SRQ-20) in primary care in the city of Sao Paulo. Br J Psychiatry 1986; 148: 23-26
    CrossrefPubMedGoogle Scholar
  • 33 Centre for Functional MRI of Brain – FMRIB. Analysis Group. . Oxford, UK. http://fsl.fmrib.ox.ac.uk/fsl/fslwiki/
    Google Scholar
  • 34 Woo CW, Krishnan A, Wager TD. Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 2014; 91: 412-419
    CrossrefPubMedGoogle Scholar
  • 35 Worsley KJ. Statistical Analysis of Activation Images. In: Matthews PM, Smith SM. Functional MRI: An Introduction to Methods. Jezzard P. 2001
    CrossrefGoogle Scholar
  • 36 Paulus MP. The role of neuroimaging for the diagnosis and treatment of anxiety disorders. Depress Anxiety 2008; 25 (04) 348-356
    CrossrefPubMedGoogle Scholar
  • 37 Etkin A, Wager TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 2007; 164 (10) 1476-1488
    CrossrefPubMedGoogle Scholar
  • 38 Sack AT. Parietal cortex and spatial cognition. Behav Brain Res 2009; 202 (02) 153-161
    CrossrefPubMedGoogle Scholar
  • 39 Rosenthal CR, Roche-Kelly EE, Husain M, Kennard C. Response-dependent contributions of human primary motor cortex and angular gyrus to manual and perceptual sequence learning. J Neurosci 2009; 29 (48) 15115-15125
    CrossrefPubMedGoogle Scholar
  • 40 Bray S, Almas R, Arnold AE, Iaria G, MacQueen G. Intraparietal sulcus activity and functional connectivity supporting spatial working memory manipulation. Cereb Cortex 2015; 25 (05) 1252-1264
    CrossrefPubMedGoogle Scholar
  • 41 Aminoff EM, Kveraga K, Bar M. The role of the parahippocampal cortex in cognition. Trends Cogn Sci 2013; 17 (08) 379-390
    CrossrefPubMedGoogle Scholar
  • 42 Swartz JR, Phan KL, Angstadt M, Klumpp H, Fitzgerald KD, Monk CS. Altered activation of the rostral anterior cingulate cortex in the context of emotional face distractors in children and adolescents with anxiety disorders. Depress Anxiety 2014; 31 (10) 870-879
    CrossrefPubMedGoogle Scholar
  • 43 Shin LM, Whalen PJ, Pitman RK. et al. An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol Psychiatry 2001; 50 (12) 932-942
    CrossrefPubMedGoogle Scholar
  • 44 Keightley ML, Chiew KS, Anderson JAE, Grady CL. Neural correlates of recognition memory for emotional faces and scenes. Soc Cogn Affect Neurosci 2011; 6 (01) 24-37
    CrossrefPubMedGoogle Scholar
  • 45 Ochsner KN, Gross JJ. The cognitive control of emotion. Trends Cogn Sci 2005; 9 (05) 242-249
    CrossrefPubMedGoogle Scholar
  • 46 Staab JP, Balaban CD, Furman JM. Threat assessment and locomotion: clinical applications of an integrated model of anxiety and postural control. Semin Neurol 2013; 33 (03) 297-306
    Article in Thieme ConnectPubMedGoogle Scholar
  • 47 Gondo M, Moriguchi Y, Kodama N. et al. Daily physical complaints and hippocampal function: an fMRI study of pain modulation by anxiety. Neuroimage 2012; 63 (03) 1011-1019
    CrossrefPubMedGoogle Scholar
  • 48 Brandt T. Phobic postural vertigo. Neurology 1996; 46 (06) 1515-1519
    CrossrefPubMedGoogle Scholar
  • 49 Paulus MP, Stein MB. An insular view of anxiety. Biol Psychiatry 2006; 60 (04) 383-387
    CrossrefPubMedGoogle Scholar
  • 50 Woll J, Sprenger A, Helmchen C. Postural control during galvanic vestibular stimulation in patients with persistent perceptual-postural dizziness. J Neurol 2019; 266 (05) 1236-1249
    CrossrefPubMedGoogle Scholar