Abstract
Purpose
Strabismus influences not only the individual with nonparallel eyes but also the observer. It has previously been demonstrated by fMRI that adults viewing images of strabismic adults have a negative reaction to the images as demonstrated by limbic activation, especially activation of the left amygdala. The aim of this study was to see if mothers would have a similar reaction to viewing strabismic children and whether or not that reaction would be different in mothers of strabismic children.
Methods
Healthy mothers of children with strabismus (n = 10, Group I) and without strabismus (n = 15, Group II) voluntarily underwent fMRI at 3T. Blood oxygen level dependent signal responses to viewing images of strabismic and non-strabismic children were analyzed.
Results
Group II, while viewing images of strabismic children, showed significantly increased activation of the limbic network (p < 0.05) and bilateral amygdala activation. Group I showed considerably less limbic activation, compared to the group II, and had no amygdala activation. Both groups revealed statically significant activation in the FEF (frontal eye field) when they were viewing images of strabismic children as compared to when they were viewing children with parallel eyes. The activated FEF area for Group II was much larger than for group I.
Conclusion
Mothers of non-strabismic children showed similar negative emotional fMRI patterns as adults did while viewing strabismic adults. Strabismus is an interpersonal organic issue for the observer, which also impacts the youngest members of our society.
Similar content being viewed by others
References
Berberat J, Jaggi GP, Wang FM, Remonda L, Killer HE. Changes in the amygdala produced by viewing strabismic eyes. Ophthalmology. 2013;120:2125–9.
Rosenbaum AL. The goal of adult strabismus surgery is not cosmetic. Arch Ophthalmol. 1999;117:250.
Hatt SR, Leske DA, Kirgis PA, Bradley EA, Holmes JM. The effects of strabismus on quality of life in adults. Am J Ophthalmol. 2007;144:643–7.
Mojon-Azzi SM, Potnik W, Mojon DS. Opinions of dating agents about strabismic subjects’ ability to find a partner. Br J Ophthalmol. 2008;92:765–9.
Mojon-Azzi SM, Mojon DS. Strabismus and employment: the opinion of headhunters. Acta Ophthalmol. 2009;87:784–8.
Costafreda SG, Brammer MJ, David AS, Fu CH. Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Res Rev. 2008;58:57–70.
Aldhafeeri FM, Mackenzie I, Kay T, Alghamdi J, Sluming V. Regional brain responses to pleasant and unpleasant IAPS pictures: different networks. Neurosci Lett. 2012;512:94–8.
Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Rosen BR. Response and habituation of the human amygdala during visual processing of facial expression. Neuron. 1996;17:875–87.
Darwin CR. The expression of the emotions in man and animals. 1st ed. London: John Murray; 1972.
Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends Cogn Sci (Regul Ed). 2000;4:223–33.
Kandel E, Schwarzt JH, Jessell TM, Siegelbaum SA, Hudspeth AJ. Principles of Neural Science. 5th ed. New York: McGraw-Hill; 2013.
Kryklywy JH, Nantes SG, Mitchell DG. The amygdala encodes level of perceived fear but not emotional ambiguity in visual scenes. Behav Brain Res. 2013;252:396–404.
Somerville LH, Kim H, Johnstone T, Alexander AL, Whalen PJ. Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety. Biol Psychiatry. 2004;55:897–903.
de Marco G, Menuel C, Guillevin R, Vallée JN, Lehmann P, Fall S, Quaglino V, Bourdin B, Devauchelle B, Chiras J. Clinical interest of fMRI and functional exploration methods of brain activity and interactivity: physical and neurophysiological considerations. J Neuroradiol. 2008;35:131–43.
Fesl G, Demmel M, Albrecht J, Kopietz R, Schoepf V, Kleemann AM, Pollatos O, Anzinger A, Schreder T, Brueckmann H, Wiesmann M. Bad mood-—bad activation? : The influence of emotions on the BOLD signal during finger tapping. Clin Neuroradiol. 2010;20:153–9.
Lane RD, Reiman EM, Bradley MM, Lang PJ, Ahern GL, Davidson RJ, Schwartz GE. Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia. 1997;35:1437–44.
Decety J, Chen C, Harenski C, Kiehl KA. An fMRI study of affective perspective taking in individuals with psychopathy: imagining another in pain does not evoke empathy. Front Hum Neurosci. 2013;24(7):489.
Adolphs R, Spezio M. Role of amygdala in processing visual social stimuli. Prog Brain Res. 2006;156:363–78.
Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Bruce R, Rosen BR. Response and habituation of the human amygdala during visual processing of facial expression. Neuron. 1996;17:875–87.
Adolphs R, Tranel D, Damasio H, Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature. 1994;372:669–72.
Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Feldman Barrett L. The brain basis of emotion: A meta-analytic review. Behav Brain Sci. 2012;35:121–43.
George N, Dolan RJ, Fink GR, Baylis GC, Russell C, Driver J. Contrast polarity and face recognition in the human fusiform gyrus. Nat Neurosci. 1999;2:574–80.
Boudiaf N, Attyé A, Warnking JM, Troprès I, Lamalle L, Pietras J, Krainik A. BOLD fMRI of cerebrovascular reactivity in the middle cerebral artery territory: A 100 volunteers’ study. J Neuroradiol. 2015;42:338–44.
Destrieux C, Hommet C, Domengie F, Boissy JM, De Marco G, Joanette Y, Andersson F, Cottier JP. Influence of age on the dynamics of fMRI activations during a semantic fluency task. J Neuroradiol. 2012;39:158–66.
Ducreux D, Marsot-Dupuch K, Lasjaunias P, Oppenheim C, Frédy D. Lyrical and musical auditive mental imagery in functional MRI. J Neuroradiol. 2003;30:18–24.
Pierrot-Deseilligny C, Muri RM, Ploner CJ, Gaymard B, Rivaud-Pechoux S. Cortical control of ocular saccades in humans: a model for motricity. Prog Brain Res. 2003;142:3–17.
Henderson JM, Williams CC, Falk RJ. Eye movements are functional during face learning. Mem Cognit. 2005;33:98–106.
Argyle M, Argyle M. Eye-contact and distance: A reply to Stephenson and Rutter. Br J Psychol. 1970;61:395–6.
Yarbus AL. Eye Movements and Vision. New York: Plenum Press; 1967.
Henderson JM, Falk R, Minut S, Dyer FC, Mahadevan S. Gaze Control for Face Learning and Recognition by Humans and Machines. In: Shipley T, Kellman P, editors. From fragments to objects: Segmentation processes in vision. 2001. pp. 463–81.
Janik SW, Wellens AR, Goldberg ML, Dell’Osso LF. Eyes as the center of focus in the visual examination of human faces. Percept Mot Skills. 1978;47:857–8.
Kingstone A. Taking a real look at social attention. Curr Opin Neurobiol. 2009;19:52–6.
Sakano N. The role of eye movements in various form of perception. Psychologia. 1963;6:215–27.
Acknowledgements
We greatly acknowledge the Aarau Cantonal Hospital Research Fond (Grant No. 1410.000.055). We have no further financial disclosures to declare.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
J. Berberat, M. Montali, P. Gruber, A. Pircher, M. Hlavica, F. Wang, H.P. Killer and L. Remonda declare that they have no competing interests.
Rights and permissions
About this article
Cite this article
Berberat, J., Montali, M., Gruber, P. et al. Modulation of the Emotional Response to Viewing Strabismic Children in Mothers—Measured by fMRI. Clin Neuroradiol 29, 87–94 (2019). https://doi.org/10.1007/s00062-017-0625-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00062-017-0625-5