Patient-Clinician Eye Contact: Social Neuroscience and Art of Clinical Engagement

References

• . Mauksch LB, Dugdale DC, Dodson S, Epstein R. Relationship, communication, and efficiency in the medical encounter: creating a clinical model from a literature review. Arch Intern Med. 2008;168(13):1387–1395
   PubMed Web of Science ®Google Scholar
• . Dyche L. Interpersonal skill in medicine: the essential partner of verbal communication. J Gen Intern Med. 2007;22(7):1035–1039
   PubMed Web of Science ®Google Scholar
• . Jones W, Carr K, Klin A. Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Arch Gen Psychiatry. 2008;65(8):946–954
   PubMed Web of Science ®Google Scholar
• . Horley K, Williams LM, Gonsalvez C, Gordon E. Social phobics do not see eye to eye: a visual scanpath study of emotional expression processing. J Anxiety Disord. 2003;17(1):33–44
   PubMed Web of Science ®Google Scholar
• . Senju A, Johnson MH. The eye contact effect: mechanisms and development. Trends Cogn Sci. 2009;13(3):127–134
   PubMed Web of Science ®Google Scholar
• . Suchman AL, Markakis K, Beckman HB, Frankel R. A model of empathic communication in the medical interview. JAMA. 1997;277(8):678–682
   PubMed Web of Science ®Google Scholar
• . Gallese V. The manifold nature of interpersonal relations: the quest for a common mechanism. Philos Trans R Soc Lond B Biol Sci. 2003;358(1431):517–528
   PubMed Web of Science ®Google Scholar
• . Larson EB, Yao X. Clinical empathy as emotional labor in the patient-physician relationship. JAMA. 2005;293(9):1100–1106
   PubMed Web of Science ®Google Scholar
• . Skuse DH, Gallagher L. Dopaminergic-neuropeptide interactions in the social brain. Trends Cogn Sci. 2009;13(1):27–35
   PubMed Web of Science ®Google Scholar
• . Porges SW. Social engagement and attachment: a phylogenetic perspective. Ann N Y Acad Sci. 2003;1008:31–17
   PubMed Web of Science ®Google Scholar
• . Insel TR, Fernald RD. How the brain processes social information: searching for the social brain. Annu Rev Neurosci. 2004;27:697–722
   PubMed Web of Science ®Google Scholar
• . Emery NJ. The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev. 2000;24(6):581–604
   PubMed Web of Science ®Google Scholar
• . Calder AJ, Lawrence AD, Keane J, . Reading the mind from eye gaze. Neuropsychologia. 2002;40(8):1129–1138
   PubMed Web of Science ®Google Scholar
• . Schulte-Rüther M, Markowitsch HJ, Fink GR, Piefke M. Mirror neuron and theory of mind mechanisms involved in face-to-face interactions: a functional magnetic resonance imaging approach to empathy. J Cogn Neurosci. 2007;19(8):1354–1372
   PubMed Web of Science ®Google Scholar
• . Adolphs R. Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behav Cogn Neurosci Rev. 2002;1(1):21–62
   PubMedGoogle Scholar
• . Vuilleumier P. Cognitive science: staring fear in the face. Nature. 2005;433(7021):22–23
   PubMedGoogle Scholar
• . Hietanen JK, Leppänen JM, Peltola MJ, Linna-Aho K, Ruuhiala HJ. Seeing direct and averted gaze activates the approach-avoidance motivational brain systems. Neuropsychologia. 2008;46(9):2423–2430
   PubMed Web of Science ®Google Scholar
• . Conty L, N'Diaye K, Tijus C, George N. When eye creates the contact! ERP evidence for early dissociation between direct and averted gaze motion processing. Neuropsychologia. 2007;45(13):3024–3037
   PubMed Web of Science ®Google Scholar
• . Demos KE, Kelley WM, Ryan SL, Davis FC, Whalen PJ. Human amygdala sensitivity to the pupil size of others. Cereb Cortex. 2008;18(12):2729–2734
   PubMedGoogle Scholar
• . Morris JS, deBonis M, Dolan RJ. Human amygdala responses to fearful eyes. Neuroimage. 2002;17(1):214–222
   PubMed Web of Science ®Google Scholar
• . Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry. 2001;42(2):241–251
   PubMed Web of Science ®Google Scholar
• . Stein MB, Goldin PR, Sareen J, Zorrilla LT, Brown GG. Increased amygdala activation to angry and contemptuous faces in generalized social phobia. Arch Gen Psychiatry. 2002;59(11):1027–1034
   PubMed Web of Science ®Google Scholar
• . Nummenmaa L, Calder AJ. Neural mechanisms of social attention. Trends Cogn Sci. 2009;13(3):135–143
   PubMed Web of Science ®Google Scholar
• . Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G. Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron. 2003;40(3):655–664
   PubMed Web of Science ®Google Scholar
• . Dadds MR, El Masry Y, Wimalaweera S, Guastella AJ. Reduced eye gaze explains “fear blindness” in childhood psychopathic traits. J Am Acad Child Adolesc Psychiatry. 2008;47(4):455–463
   PubMed Web of Science ®Google Scholar
• . Vuilleumier P. How brains beware: neural mechanisms of emotional attention. Trends Cogn Sci. 2005;9(12):585–594
   PubMed Web of Science ®Google Scholar
• . LeDoux JE. The Emotional Brain. New York, NY: Simon and Schuster; 1996
   Google Scholar
• . Rolls ET, O'Doherty J, Kringelbach ML, Francis S, Bowtell R, McGlone F. Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cereb Cortex. 2003;13(3): 308–317
   PubMed Web of Science ®Google Scholar
• . Bechara A. Naqvi N. Listening to your heart: interoceptive awareness as a gateway to feeling. Nat Neurosci. 2004;7(2):102–103
   PubMedGoogle Scholar
• . Winston JS, Strange BA, O'Doherty J, Dolan RJ. Automatic and intentional brain responses during evaluation of trustworthiness of faces. Nat Neurosci. 2002;5(3):277–283
   PubMed Web of Science ®Google Scholar
• . Dadds MR, Perry Y, Hawes DJ, . Attention to the eyes and fear-recognition deficits in child psychopathy. Br J Psychiatry. 2006;189:280–281
   PubMed Web of Science ®Google Scholar
• . Dadds MR, Rhodes T. Aggression in young children with concurrent callous-unemotional traits: can the neurosciences inform progress and innovation in treatment approaches? Philos Trans R Soc Lond B Biol Sci. 2008;63(1503):2567–2576
   Google Scholar
• . Marsh AA, Finger EC, Mitchell DG, . Reduced amygdala response to fearful expressions in children and adolescents with callous unemotional traits and disruptive behavior disorders. Am J Psychiatry. 2008;165(6):712–720
   PubMed Web of Science ®Google Scholar
• . Stein MB, Simmons AN, Feinstein JS, Paulus MP. Increased amygdala and insula activation during emotion processing in anxiety prone subjects. Am J Psychiatry. 2007;164(2):318–327
   PubMed Web of Science ®Google Scholar
• . Monk CS, Klein RG, Telzer EH, . Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression. Am J Psychiatry. 2008;165(1):90–98
   PubMed Web of Science ®Google Scholar
• . Caspi A, Sugden K, Moffitt TE, . Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003;301(5631):386–389
   PubMed Web of Science ®Google Scholar
• . Cools R, Calder AJ, Lawrence AD, Clark L, Bullmore E, Robbins TW. Individual differences in threat sensitivity predict serotonergic modulation of amygdala response to fearful faces. Psychopharmacology (Berl). 2005;180(4):670–679
   PubMedGoogle Scholar
• . Todorov A. Evaluating faces on trustworthiness: an extension of systems for recognition of emotions signaling approach/avoidance behaviors. Ann N Y Acad Sci. 2008;1124:208–224
   PubMed Web of Science ®Google Scholar
• . Haxby JV, Hoffman EA, Gobbini MI. Human neural systems for face recognition and social communication. Biol Psychiatry. 2002;51(1):59–67
   PubMed Web of Science ®Google Scholar
• . Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol. 2002;12(2):169–177
   PubMed Web of Science ®Google Scholar
• . Whalen PJ, Kagan J, Cook RG, . Human amygdala responsivity to masked fearful eye whites. Science. 2004;306(5704):2061
   PubMed Web of Science ®Google Scholar
• . Kingstone A, Tipper C, Ristic J, Ngan E. The eyes have it!: an fMRI investigation. Brain Cogn. 2004;55(2):269–271
   PubMed Web of Science ®Google Scholar
• . Nagasawa M, Kikusui T, Onaka T, Ohta M. Dog's gaze at its owner increases owner's urinary oxytocin during social interaction. Horm Behav. 2009;55(3):434–441
   PubMed Web of Science ®Google Scholar
• . Stern D. The Present Moment in Psychotherapy and Everyday Life. New York, NY: W. W. Norton and Company; 2004
   Google Scholar
• . Mena MA, de Yébenes JG. Drug-induced parkinsonism. Expert Opin Drug Saf. 2006;5(6):759–771
   PubMed Web of Science ®Google Scholar
• . Weiner WJ. Early diagnosis of Parkinson's disease and initiation of treatment. Rev Neurol Dis. 2008;5(2):46–53
   PubMedGoogle Scholar
• . Tse WS, Bond AJ. Serotonergic intervention affects both social dominance and affiliative behaviour. Psychopharmacology (Berl). 2002;161(3):324–330
   PubMed Web of Science ®Google Scholar
• . Tse WS, Bond AJ. Reboxetine promotes social bonding in healthy volunteers. J Psychopharmacol. 2003;17(2):189–195
   PubMedGoogle Scholar
• . Browning M, Reid C, Cowen PJ, Goodwin GM, Harmer CJ. A single dose of citalopram increases fear recognition in healthy subjects. J Psychopharmacol. 2007;21(7):684–690
   PubMedGoogle Scholar
• . Furmark T, Tillfors M, Marteinsdottir I, . Common changes in cerebral blood flow in patients with social phobia treated with citalopram or cognitive-behavioral therapy. Arch Gen Psychiatry. 2002;59(5):425–433
   PubMed Web of Science ®Google Scholar
• . Paulus MP, Feinstein JS, Castillo G, Simmons AN, Stein MB. Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. Arch Gen Psychiatry. 2005;62(3):282–288
   PubMed Web of Science ®Google Scholar
• . Furmark T, Tillfors M, Garpenstrand H, . Serotonin transporter polymorphism related to amygdala excitability and symptom severity in patients with social phobia. Neurosci Lett. 2004;362(3):189–192
   PubMedGoogle Scholar
• . Hariri AR, Drabant EM, Munoz KE, . A susceptibility gene for affective disorders and the response of the human amygdala. Arch Gen Psychiatry. 2005;62(2):146–152
   PubMed Web of Science ®Google Scholar
• . Farroni T, Csibra G, Simion F, Johnson MH. Eye contact detection in humans from birth. Proc Natl Acad Sci U S A. 2002;99(14): 9602–9605
   PubMed Web of Science ®Google Scholar
• . Schore AN. Affect Regulation and the Disorders of the Self. New York, NY: W. W. Norton and Company; 2003
   Google Scholar
• . Brass M, Heyes C. Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn Sci. 2005;9(10):489–495
   PubMed Web of Science ®Google Scholar
• . Oberman LM, Pineda JA, Ramachandran VS. The human mirror neuron system: a link between action observation and social skills. Soc Cogn Affect Neurosci. 2007;2(1):62–66
   PubMed Web of Science ®Google Scholar
• . Carter CS, Grippo AJ, Pournajafi-Nazarloo H, Ruscio MG, Porges SW. Oxytocin, vasopressin and sociality. Prog Brain Res. 2008;170:331–336
   PubMed Web of Science ®Google Scholar
• . Heinrichs M, Domes G. Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans. Prog Brain Res. 2008;170:337–350
   PubMed Web of Science ®Google Scholar
• . Ditzen B, Hoppmann C, Klumb P. Positive couple interactions and daily cortisol: on the stress-protecting role of intimacy. Psychosom Med, 2008;70(8):883–889
   PubMed Web of Science ®Google Scholar
• . Petrovic P, Kalisch R, Singer T, Dolan RJ. Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci. 2008;28(26):6607–6615
   PubMed Web of Science ®Google Scholar
• . Guastella AJ, Mitchell PB, Dadds MR. Oxytocin increases gaze to the eye region of human faces. Biol Psychiatry. 2008;63(1):3–5
   PubMed Web of Science ®Google Scholar
• . Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. Oxytocin improves “mind-reading” in humans. Biol Psychiatry. 2007;61(6):731–733
   PubMed Web of Science ®Google Scholar
• . Lerer E, Levi S, Salomon S, Darvasi A, Yirmiya N, Ebstein RP. Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition. Mol Psychiatry. 2007;13(10):980–988
   PubMedGoogle Scholar
• . Hollander E, Bartz J, Chaplin W, . Oxytocin increases retention of social cognition in autism. Biol Psychiatry. 2007;61(4):498–503
   PubMed Web of Science ®Google Scholar
• . Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M. Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. J Child Psychol Psychiatry. 1997;38(7):813–822
   PubMed Web of Science ®Google Scholar
• . Girón M, Manjón-Arce P, Puerto-Barber J, Sánchez-García E, Gómez-Beneyto M. Clinical interview skills and identification of emotional disorders in primary care. Am J Psychiatry. 1998;155(4):530–535
   PubMedGoogle Scholar
• . Kettle JW, O'Brien-Simpson L, Allen NB. Impaired theory of mind in first-episode schizophrenia: comparison with community, university and depressed controls. Schizophr Res. 2008;99(1-3):96–102
   PubMedGoogle Scholar
• . Gregory C, Lough S, Stone V, . Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer's disease: theoretical and practical implications. Brain. 2002;125(pt 4):752–764
   PubMed Web of Science ®Google Scholar
• . Stone VE, Baron-Cohen S, Calder A, Keane J, Young A. Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia. 2003;41(2):209–220
   PubMed Web of Science ®Google Scholar
• . Keltner D. Expression and the course of life: studies of emotion, personality, and psychopathology from a social-functional perspective. Ann N Y Acad Sci. 2003;1000:222–243
   PubMed Web of Science ®Google Scholar
• . Wieser MJ, Pauli P, Alpers GW, Mühlberger A. Is eye to eye contact really threatening and avoided in social anxiety? An eye-tracking and psychophysiology study. J Anxiety Disord. 2009;23(1):93–103
   PubMed Web of Science ®Google Scholar
• . Troisi A, Pasini A, Bersani G, Di Mauro M, Ciani N. Negative symptoms and visual behavior in DSM-III-R prognostic subtypes of schizophreniform disorder. Acta Psychiatr Scand. 1991;83(5):391–394
   PubMedGoogle Scholar
• . Franck N, Montoute T, Labruyère N, . Gaze direction determination in schizophrenia. Schizophr Res. 2002;56(3):225–234
   PubMedGoogle Scholar
• . Meyer-Lindenberg A, Hariri AR, Munoz KE, . Neural correlates of genetically abnormal social cognition in Williams syndrome. Nat Neurosci. 2005;8(8):991–993
   PubMed Web of Science ®Google Scholar
• . Watson C, Hoeft F, Garrett AS, Hall SS, Reiss AL. Aberrant brain activation during gaze processing in boys with fragile x syndrome. Arch Gen Psychiatry. 2008;65(11):1315–1323
   PubMedGoogle Scholar
• . Adolphs R, Baron-Cohen S, Tranel D. Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci. 2002;14(8):1264–1274
   PubMed Web of Science ®Google Scholar
• . Tomkins S. Affect Imagery Consciousness The Negative Affects. Vol 2. New York, NY: Springer Publishing; 1963
   Google Scholar
• . Panksepp J. Why does separation distress hurt? Comment on MacDonald and Leary (2005). Psychol Bull. 2005;131(2):224–230
   PubMedGoogle Scholar
• . Rüsch N, Lieb K, Göttler I, . Shame and implicit self-concept in women with borderline personality disorder. Am J Psychiatry. 2007;164(3):500–508
   PubMed Web of Science ®Google Scholar
• . Napieralski LP, Brooks CI, Droney JM. The effect of duration of eye contact on American college students' attributions of state, trait, and test anxiety. J Soc Psychol. 1995;135(3):273–280
   PubMed Web of Science ®Google Scholar
• . Deladisma AM, Cohen M, Stevens A, ; Association for Surgical Education. Do medical students respond empathetically to a virtual patient? Am J Surg. 2007;193(6):756–760
   PubMed Web of Science ®Google Scholar
• . Mason MF, Hood BM, Macrae CN. Look into my eyes: gaze direction and person memory. Memory. 2004;12(5):637–643
   PubMed Web of Science ®Google Scholar
• . Kampe KK, Frith CD, Frith U. “Hey John”: signals conveying communicative intention toward the self activate brain regions associated with “mentalizing,” regardless of modality. J Neurosci. 2003;23(12):5258–5263
   PubMed Web of Science ®Google Scholar
• . Adams RB Jr, Kleck RE. Effects of direct and averted gaze on the perception of facially communicated emotion. Emotion. 2005;5(1):3–11
   PubMed Web of Science ®Google Scholar
• . Dolcos F, LaBar KS, Cabeza R. Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proc Natl Acad Sci U S A. 2005;102(7):2626–2631
   PubMed Web of Science ®Google Scholar
• . Churchill LR, Schenck D. Healing skills for medical practice. Ann Intern Med. 2008;149(10):720–724
   PubMed Web of Science ®Google Scholar
• . Preston SD, de Waal FB. Empathy: its ultimate and proximate bases. Behav Brain Sci. 2002;25(1):1–20
   PubMed Web of Science ®Google Scholar
• . Botvinick M, Jha AP, Bylsma LM, Fabian SA, Solomon PE, Prkachin KM. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage. 2005;25(1):312–319
   PubMed Web of Science ®Google Scholar
• . Beauregard M. Mind does really matter: evidence from neuroimaging studies of emotional self-regulation, psychotherapy, and placebo effect. Prog Neurobiol. 2007;81(4):218–236
   PubMed Web of Science ®Google Scholar
• . Enck P, Klosterhalfen S. The story of O-is oxytocin the mediator of the placebo response? Neurogastroenterol Motil. 2009;21(4):347–350
   PubMedGoogle Scholar