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The autonomic and behavioral profile of emotional dysregulation

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The autonomic and behavioral profile ofemotional dysregulationJ.D. Woolley, BS; M.L. Gorno-Tempini, MD, PhD*; K. Werner, BS*; K.P. Rankin, PhD; P. Ekman, PhD;R.W. Levenson, PhD; and B.L. Miller, MDAbstract—The authors describe a patient with focal brain atrophy and emotional lability characterized by episodes ofexcessive crying and laughing. The patient was selectively impaired in the production of voluntary complex facialmovements and was unable to regulate her emotional behavior and autonomic reactivity. She also displayed increasedbehavioral and autonomic changes when explicitly trying to suppress her responses to emotional stimuli (compared withwhen not trying to regulate her responses). This pattern of deficits supports a selective deficit in voluntary emotionalcontrol.NEUROLOGY 2004;63:1740 –1743Human emotions help coordinate responses to evolu-tionarily relevant prototypic scenarios, such asthreat.1Emotions are associated with specific auto-nomic profiles2and stereotyped facial expressionsthat are recognized by members of all cultures3andare produced even by congenitally blind infants.4At-tempts to voluntarily suppress emotional displays af-fect the magnitude of behavioral and autonomicresponses to the emotional stimuli.5,6Although is-sues of lateralization remain unclear, the prefrontalcortex has repeatedly been implicated in voluntaryemotion regulation.7-9The mechanisms that producecoordinated multisystem emotional responses can bedisrupted, as seen in emotional dysregulation associ-ated with bipolar disorder, schizophrenia, and fron-totemporal dementia. New psychological andautonomic tools recently have been developed tostudy emotional responses in normal individuals. Wehave adapted these techniques to quantify the emo-tional deficits in a patient with neurodegenerativedisease and symptoms of emotional lability.Case report. The patient is a 69-year-old woman who was ex-amined for a 5-year history of slowly progressing mutism andemotional lability. Using structural MRI and PET, we identifiedspecific regions of cortical atrophy and hypometabolism. In partic-ular, these imaging studies demonstrated significant (left greaterthan right) inferior frontal gyrus damage (figure 1). On examina-tion, she had focal deficits in the ability to follow commands toproduce or to imitate complex oral-buccal movements (buccofacialapraxia) and a complete inability to speak. Other cognitive do-mains, including language comprehension, memory, recognition ofemotion from faces and prosodic cues, and semantic knowledge ofemotion, were remarkably preserved (see E-Methods and tablesE-1 and E-2 on the Neurology Web site at www.neurology.org).Her presentation suggested a syndrome of focal cortical atrophycaused by a neurodegenerative disease, possibly cortical basaldegeneration.To quantify the patient’s emotional deficits, we assessed hermotor and autonomic responses to disgust-eliciting films (war sur-geries and burn-victim treatments) and sudden unexpected noises(acoustic startle). Unlike other negative emotions that producemarked increases in cardiac activation, such as fear and anger,disgust typically produces only moderate changes (often smalldecreases), likely reflecting vagal influence on this emotional re-sponse.2When normal subjects are asked to suppress the behav-ioral signs of emotion in response to a disgusting film, they exhibitsharply diminished behavioral signs of disgust and sharp in-creases in cardiovascular activation.5While watching a disgusting film and not instructed to modu-late expressive behavior (“Non Suppress”), the patient’s expres-sive behavior and cardiac physiologic responses were comparablewith control subjects (figure 2). However, when asked to hide herfeelings while watching another disgusting film (“Suppress”), sheshowed significantly more expressive behavior (shaking her headand silently mouthing the word “terrible”) and a significant de-crease in cardiac response vs control subjects. The patient re-ported that she had tried to suppress her response, indicating thatshe had understood the instructions; she stated that she had beenmoderately successful.The patient’s responses to acoustic startle stimuli were alsoatypical. When this noxious stimulus is presented without warn-ing, it produces marked increases in cardiovascular activation andlarge behavioral responses.5If control subjects are told when thestartle stimulus will occur, however, they “brace” themselves, andthe behavioral response is significantly reduced, and the cardio-vascular response is increased.6The patient’s behavioral re-sponses to the warned startle were increased when compared withher responses to the unwarned startle. She also demonstrateddecreased cardiovascular activation when warned.To assess our patient’s voluntary control of facial movement,we conducted a number of tests. Using the Facial Action CodingSystem, we assessed her ability to make individual facial move-Additional material related to this article can be found on the NeurologyWeb site. Go to www.neurology.org and scroll down the Table of Con-tents for the November 9 issue to find the link for this article.*These authors contributed equally to this work.From the Department of Neurology (Drs. Gorno-Tempini, Rankin, and Miller, J.D. Woolley), University of California, San Francisco; Department ofPsychology (Dr. Levenson, K. Werner), University of California, Berkeley; and Human Interaction Laboratory (Dr. Ekman), University of California, SanFrancisco, CA.Supported by the following grants: NIA grants P50-AG05142, AG16570, AG 19724-FTD PPG, and ADRC AG023501.Received January 13, 2004. Accepted in final form July 1, 2004.Address correspondence and reprint requests to Dr. B.L. Miller, Department of Neurology, University of California San Francisco, 350 Parnassus Street,Suite 706, San Francisco, CA 94143-1207; e-mail: [email protected] Copyright © 2004 by AAN Enterprises, Inc.ments singly and in pairs (see table E-3 on the Neurology Website). She was able to make many small simple facial movements,including opening and closing her eyes and moving her eyebrows,but was unable to combine two or more single movements intomore complex movements. Tests of facial praxis revealed a similarinability to produce complex facial movements. The patient wasunable to pretend to puff on a pipe, suck on a straw, or smoke acigarette to command or to imitation. Her facial performance im-proved when the actions were


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