Semin Speech Lang 2018; 39(01): 087-100
DOI: 10.1055/s-0037-1608859
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Impaired Recognition of Emotional Faces after Stroke Involving Right Amygdala or Insula

Donna C. Tippett
1   Department of Neurology, Johns Hopkins University School of Medicine, Baltimore Maryland
2   Department of Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore Maryland
3   Department of Otolaryngology–Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore Maryland
,
Brittany R. Godin
4   Rehabilitation Services, University of Maryland Charles Regional Medical Center, La Plata, Maryland
,
Kumiko Oishi
5   Center for Imaging Science, Whiting School of Engineering, Johns Hopkins University, Baltimore, Maryland
,
Kenichi Oishi
6   Department of Radiology, Johns Hopkins University School of Medicine, Baltimore Maryland
,
Cameron Davis
1   Department of Neurology, Johns Hopkins University School of Medicine, Baltimore Maryland
,
Yessenia Gomez
1   Department of Neurology, Johns Hopkins University School of Medicine, Baltimore Maryland
,
Lydia A. Trupe
1   Department of Neurology, Johns Hopkins University School of Medicine, Baltimore Maryland
,
Eun Hye Kim
1   Department of Neurology, Johns Hopkins University School of Medicine, Baltimore Maryland
,
Argye E. Hillis
1   Department of Neurology, Johns Hopkins University School of Medicine, Baltimore Maryland
3   Department of Otolaryngology–Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore Maryland
7   Department of Cognitive Science, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, Maryland
› Author Affiliations
Further Information

Publication History

Publication Date:
22 January 2018 (online)

Abstract

Despite its basic and translational importance, the neural circuitry supporting the perception of emotional faces remains incompletely understood. Functional imaging studies and chronic lesion studies indicate distinct roles of the amygdala and insula in recognition of fear and disgust in facial expressions, whereas intracranial encephalography studies, which are not encumbered by variations in human anatomy, indicate a somewhat different role of these structures. In this article, we leveraged lesion-mapping techniques in individuals with acute right hemisphere stroke to investigate lesions associated with impaired recognition of prototypic emotional faces before significant neural reorganization can occur during recovery from stroke. Right hemisphere stroke patients were significantly less accurate than controls on a test of emotional facial recognition for both positive and negative emotions. Patients with right amygdala or anterior insula lesions had significantly lower scores than other right hemisphere stroke patients on recognition of angry and happy faces. Lesion volume within several regions, including the right amygdala and anterior insula, each independently contributed to the error rate in recognition of individual emotions. Results provide additional support for a necessary role of the right amygdala and anterior insula within a network of regions underlying recognition of facial expressions, particularly those that have biological importance or motivational relevance and have implications for clinical practice.

 
  • References

  • 1 Dimberg U, Thunberg M, Elmehed K. Unconscious facial reactions to emotional facial expressions. Psychol Sci 2000; 11 (01) 86-89
  • 2 Petrides K, Furnham A. Trait emotional intelligence: behavioural validation in two studies of emotion recognition and reactivity to mood induction. Eur J Pers 2003; 17 (01) 39-57
  • 3 Braun M, Traue HC, Frisch S, Deighton RM, Kessler H. Emotion recognition in stroke patients with left and right hemispheric lesion: results with a new instrument-the FEEL Test. Brain Cogn 2005; 58 (02) 193-201
  • 4 Cheung CC, Lee TM, Yip JT, King KE, Li LS. The differential effects of thalamus and basal ganglia on facial emotion recognition. Brain Cogn 2006; 61 (03) 262-268
  • 5 Pell MD. Cerebral mechanisms for understanding emotional prosody in speech. Brain Lang 2006; 96 (02) 221-234
  • 6 Harciarek M, Heilman KM. The contribution of anterior and posterior regions of the right hemisphere to the recognition of emotional faces. J Clin Exp Neuropsychol 2009; 31 (03) 322-330
  • 7 Blonder LX, Pettigrew LC, Kryscio RJ. Emotion recognition and marital satisfaction in stroke. J Clin Exp Neuropsychol 2012; 34 (06) 634-642
  • 8 Bowers D, Bauer RM, Coslett HB, Heilman KM. Processing of faces by patients with unilateral hemisphere lesions. I. Dissociation between judgments of facial affect and facial identity. Brain Cogn 1985; 4 (03) 258-272
  • 9 Blonder LX, Bowers D, Heilman KM. The role of the right hemisphere in emotional communication. Brain 1991; 114 (Pt 3): 1115-1127
  • 10 Abbott JD, Wijeratne T, Hughes A, Perre D, Lindell AK. The influence of left and right hemisphere brain damage on configural and featural processing of affective faces. Laterality 2014; 19 (04) 455-472
  • 11 Breiter HC, Etcoff NL, Whalen PJ. , et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996; 17 (05) 875-887
  • 12 Fusar-Poli P, Placentino A, Carletti F. , et al. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 2009; 34 (06) 418-432
  • 13 Hughlings-Jackson J. On the nature of duality of the brain. Brain 1915; 38: 96-103
  • 14 Borod J. The Neurophysiology of Emotion. New York, NY: Oxford University Press; 2000
  • 15 Yip JT, Leung KK, Li LS, Lee TM. The role of sub-cortical brain structures in emotion recognition. Brain Inj 2004; 18 (12) 1209-1217
  • 16 Langer SL, Pettigrew LC, Wilson JF, Blonder LX. Personality and social competency following unilateral stroke. J Int Neuropsychol Soc 1998; 4 (05) 447-455
  • 17 Davidson RJ, Shackman AJ, Maxwell JS. Asymmetries in face and brain related to emotion. Trends Cogn Sci 2004; 8 (09) 389-391
  • 18 Abbott JD, Wijeratne T, Hughes A, Perre D, Lindell AK. The influence of left and right hemisphere brain damage on configural and featural processing of affective faces. Laterality 2014; 19 (04) 455-472
  • 19 Thomas NA, Wignall SJ, Loetscher T, Nicholls ME. Searching the expressive face: evidence for both the right hemisphere and valence-specific hypotheses. Emotion 2014; 14 (05) 962-977
  • 20 Calvo MG, Beltrán D. Brain lateralization of holistic versus analytic processing of emotional facial expressions. Neuroimage 2014; 92: 237-247
  • 21 Hitchcock J, Davis M. Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci 1986; 100 (01) 11-22
  • 22 Paré D, Quirk GJ, Ledoux JE. New vistas on amygdala networks in conditioned fear. J Neurophysiol 2004; 92 (01) 1-9
  • 23 Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF. The brain basis of emotion: a meta-analytic review. Behav Brain Sci 2012; 35 (03) 121-143
  • 24 Schneider S, Peters J, Bromberg U. , et al; IMAGEN consortium. Boys do it the right way: sex-dependent amygdala lateralization during face processing in adolescents. Neuroimage 2011; 56 (03) 1847-1853
  • 25 Almeida I, van Asselen M, Castelo-Branco M. The role of the amygdala and the basal ganglia in visual processing of central vs. peripheral emotional content. Neuropsychologia 2013; 51 (11) 2120-2129
  • 26 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 (6507): 669-672
  • 27 Adolphs R, Tranel D, Damasio H, Damasio AR. Fear and the human amygdala. J Neurosci 1995; 15 (09) 5879-5891
  • 28 Calder AJ, Young AW, Rowland D, Perrett DI, Hodges JR, Etcoff NL. Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear. Cogn Neuropsychol 1996; 13 (05) 699-745
  • 29 Sprengelmeyer R, Young AW, Schroeder U. , et al. Knowing no fear. Proc Biol Sci 1999; 266 (1437): 2451-2456
  • 30 Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR. A mechanism for impaired fear recognition after amygdala damage. Nature 2005; 433 (7021): 68-72
  • 31 Wolf RC, Philippi CL, Motzkin JC, Baskaya MK, Koenigs M. Ventromedial prefrontal cortex mediates visual attention during facial emotion recognition. Brain 2014; 137 (Pt 6): 1772-1780
  • 32 Kumfor F, Irish M, Hodges JR, Piguet O. Discrete neural correlates for the recognition of negative emotions: Insights from frontotemporal dementia. PLoS One 2013; 8 (06) e67457
  • 33 Oliver LD, Virani K, Finger EC, Mitchell DG. Is the emotion recognition deficit associated with frontotemporal dementia caused by selective inattention to diagnostic facial features?. Neuropsychologia 2014; 60: 84-92
  • 34 Hot P, Klein-Koerkamp Y, Borg C. , et al. Fear recognition impairment in early-stage Alzheimer's disease: when focusing on the eyes region improves performance. Brain Cogn 2013; 82 (01) 25-34
  • 35 Adolphs R. What does the amygdala contribute to social cognition?. Ann N Y Acad Sci 2010; 1191 (01) 42-61
  • 36 Gorno-Tempini ML, Pradelli S, Serafini M. , et al. Explicit and incidental facial expression processing: an fMRI study. Neuroimage 2001; 14 (02) 465-473
  • 37 Harris RJ, Young AW, Andrews TJ. Dynamic stimuli demonstrate a categorical representation of facial expression in the amygdala. Neuropsychologia 2014; 56: 47-52
  • 38 Jansma H, Roebroeck A, Münte TF. A network analysis of audiovisual affective speech perception. Neuroscience 2014; 256: 230-241
  • 39 Milesi V, Cekic S, Péron J. , et al. Multimodal emotion perception after anterior temporal lobectomy (ATL). Front Hum Neurosci 2014; 8: 275
  • 40 Reynaud E, Guedj E, Trousselard M. , et al. Acute stress disorder modifies cerebral activity of amygdala and prefrontal cortex. Cogn Neurosci 2015; 6 (01) 39-43
  • 41 Atkinson AP, Adolphs R. The neuropsychology of face perception: beyond simple dissociations and functional selectivity. Philos Trans R Soc Lond B Biol Sci 2011; 366 (1571): 1726-1738
  • 42 Gamer M, Büchel C. Amygdala activation predicts gaze toward fearful eyes. J Neurosci 2009; 29 (28) 9123-9126
  • 43 Philippi CL, Mehta S, Grabowski T, Adolphs R, Rudrauf D. Damage to association fiber tracts impairs recognition of the facial expression of emotion. J Neurosci 2009; 29 (48) 15089-15099
  • 44 Phillips ML, Young AW, Scott SK. , et al. Neural responses to facial and vocal expressions of fear and disgust. Proc Biol Sci 1998; 265 (1408): 1809-1817
  • 45 Jehna M, Neuper C, Ischebeck A. , et al. The functional correlates of face perception and recognition of emotional facial expressions as evidenced by fMRI. Brain Res 2011; 1393: 73-83
  • 46 Calder AJ, Keane J, Manes F, Antoun N, Young AW. Impaired recognition and experience of disgust following brain injury. Nat Neurosci 2000; 3 (11) 1077-1078
  • 47 Kipps CM, Duggins AJ, McCusker EA, Calder AJ. Disgust and happiness recognition correlate with anteroventral insula and amygdala volume respectively in preclinical Huntington's disease. J Cogn Neurosci 2007; 19 (07) 1206-1217
  • 48 Omar R, Rohrer JD, Hailstone JC, Warren JD. Structural neuroanatomy of face processing in frontotemporal lobar degeneration. J Neurol Neurosurg Psychiatry 2011; 82 (12) 1341-1343
  • 49 Jacobs DH, Shuren J, Bowers D, Heilman KM. Emotional facial imagery, perception, and expression in Parkinson's disease. Neurology 1995; 45 (09) 1696-1702
  • 50 Dogan I, Saß C, Mirzazade S. , et al. Neural correlates of impaired emotion processing in manifest Huntington's disease. Soc Cogn Affect Neurosci 2014; 9 (05) 671-680
  • 51 Murray RJ, Brosch T, Sander D. The functional profile of the human amygdala in affective processing: insights from intracranial recordings. Cortex 2014; 60: 10-33
  • 52 Fried I, MacDonald KA, Wilson CL. Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 1997; 18 (05) 753-765
  • 53 Rutishauser U, Tudusciuc O, Neumann D. , et al. Single-unit responses selective for whole faces in the human amygdala. Curr Biol 2011; 21 (19) 1654-1660
  • 54 Krolak-Salmon P, Hénaff MA, Vighetto A, Bertrand O, Mauguière F. Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: a depth electrode ERP study in human. Neuron 2004; 42 (04) 665-676
  • 55 Blair RJ, Morris JS, Frith CD, Perrett DI, Dolan RJ. Dissociable neural responses to facial expressions of sadness and anger. Brain 1999; 122 (Pt 5): 883-893
  • 56 Harmer CJ, Thilo KV, Rothwell JC, Goodwin GM. Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions. Nat Neurosci 2001; 4 (01) 17-18
  • 57 Fellows LK, Heberlein AS, Morales DA, Shivde G, Waller S, Wu DH. Method matters: an empirical study of impact in cognitive neuroscience. J Cogn Neurosci 2005; 17 (06) 850-858
  • 58 Wittsack HJ, Ritzl A, Fink GR. , et al. MR imaging in acute stroke: diffusion-weighted and perfusion imaging parameters for predicting infarct size. Radiology 2002; 222 (02) 397-403
  • 59 Kuhl CK, Textor J, Gieseke J. , et al. Acute and subacute ischemic stroke at high-field-strength (3.0-T) diffusion-weighted MR imaging: intraindividual comparative study. Radiology 2005; 234 (02) 509-516
  • 60 Oishi K, Faria A, Jiang H. , et al. Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer's disease participants. Neuroimage 2009; 46 (02) 486-499
  • 61 Leigh R, Oishi K, Hsu J. , et al. Acute lesions that impair affective empathy. Brain 2013; 136 (Pt 8): 2539-2549
  • 62 Dara C, Kirsch-Darrow L, Ochfeld E. , et al. Impaired emotion processing from vocal and facial cues in frontotemporal dementia compared to right hemisphere stroke. Neurocase 2013; 19 (06) 521-529
  • 63 Pell MD, Leonard CL. Facial expression decoding in early Parkinson's disease. Brain Res Cogn Brain Res 2005; 23 (2–3): 327-340
  • 64 Gur RC, Schroeder L, Turner T. , et al. Brain activation during facial emotion processing. Neuroimage 2002; 16 (3 Pt 1): 651-662
  • 65 Calvo MG, Lundqvist D. Facial expressions of emotion (KDEF): identification under different display-duration conditions. Behav Res Methods 2008; 40 (01) 109-115
  • 66 Limbrecht-Ecklundt K, Scheck A, Jerg-Bretzke L, Walter S, Hoffmann H, Traue HC. The effect of forced choice on facial emotion recognition: a comparison to open verbal classification of emotion labels. Psychosoc Med 2013; 10: Doc04
  • 67 Calvo MG, Beltrán D. Recognition advantage of happy faces: tracing the neurocognitive processes. Neuropsychologia 2013; 51 (11) 2051-2061
  • 68 Bombari D, Schmid PC, Schmid Mast M, Birri S, Mast FW, Lobmaier JS. Emotion recognition: the role of featural and configural face information. Q J Exp Psychol (Hove) 2013; 66 (12) 2426-2442
  • 69 Pohl A, Anders S, Schulte-Rüther M, Mathiak K, Kircher T. Positive facial affect—an fMRI study on the involvement of insula and amygdala. PLoS One 2013; 8 (08) e69886
  • 70 Johnson SA, Stout JC, Solomon AC. , et al; Predict-HD Investigators of the Huntington Study Group. Beyond disgust: impaired recognition of negative emotions prior to diagnosis in Huntington's disease. Brain 2007; 130 (Pt 7): 1732-1744
  • 71 Calvo MG, Avero P, Fernández-Martín A, Recio G. Recognition thresholds for static and dynamic emotional faces. Emotion 2016; 16 (08) 1186-1200
  • 72 Takeda A, Kobayakawa M, Suzuki A, Tsuruya N, Kawamura M. Lowered sensitivity to facial emotions in myotonic dystrophy type 1. J Neurol Sci 2009; 280 (1–2): 35-39
  • 73 Mike A, Strammer E, Aradi M. , et al. Disconnection mechanism and regional cortical atrophy contribute to impaired processing of facial expressions and theory of mind in multiple sclerosis: a structural MRI study. PLoS One 2013; 8 (12) e82422
  • 74 Sato W, Uono S, Matsuura N, Toichi M. Misrecognition of facial expressions in delinquents. Child Adolesc Psychiatry Ment Health 2009; 3 (01) 27
  • 75 Kennedy DP, Adolphs R. Perception of emotions from facial expressions in high-functioning adults with autism. Neuropsychologia 2012; 50 (14) 3313-3319
  • 76 Statucka M, Walder DJ. Efficacy of social cognition remediation programs targeting facial affect recognition deficits in schizophrenia: a review and consideration of high-risk samples and sex differences. Psychiatry Res 2013; 206 (2-3): 125-139
  • 77 Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol 2002; 12 (02) 169-177