Brain Advance Access originally published online on November 8, 2006
Brain 2006 129(12):3356-3365; doi:10.1093/brain/awl301
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Startling facts about emotion in Parkinson's disease: blunted reactivity to aversive stimuli
1 Department of Clinical and Health Psychology , McKnight Brain Institute, University of Florida Gainesville, FL, USA 2 Department of Neurology, McKnight Brain Institute, University of Florida Gainesville, FL, USA 3 Department of Neurological Surgery, McKnight Brain Institute, University of Florida Gainesville, FL, USA 4 Movement Disorders Center, McKnight Brain Institute, University of Florida Gainesville, FL, USA
Correspondence to: Dr Dawn Bowers, Department of Clinical and Health Psychology, PO Box 100165, University of Florida Health Science Center, Gainesville, FL 32610, USA E-mail: dbowers{at}phhp.ufl.edu
The amygdala is closely linked to basal ganglia circuitry and plays a key role in danger detection and fear-potentiated startle. Based on recent findings of amygdalar abnormalities in Parkinson's disease, we hypothesized that non-demented patients with this illness would show blunted reactivity during aversive/unpleasant events, as indexed by diminished emotional modulation of the startle eyeblink response. To test this hypothesis, 23 idiopathic patients with Parkinson's disease and 17 controls viewed standardized sets of aversive, pleasant and neutral pictures for 6 s each. During this time, white noise bursts (50 ms, 95 db) were binaurally presented to elicit startle eyeblink responses, measured from electrodes over the orbicularis oculi. After viewing each picture, subjects provided ratings of valence and arousal. The Parkinson's disease patients were in the early to middle stages of their disease, not demented or depressed, and were tested ‘on’ dopaminergic medication. The two groups were similar in age, education, gender and cognitive screening status. The control group had larger startle responses when viewing negative, aversive pictures than neutral or pleasant pictures. As predicted, startle enhancement during aversive pictures was significantly muted in the Parkinson's disease patients. This blunting was not due to abnormalities in the mechanics of the startle eyeblink per se. Nor was it related to depression symptoms, medications (psychotropics), or failure to perceive/appreciate the negative meaning of aversive pictures (i.e. normal valence ratings). Reduced startle reactivity in the disease group was related to disease severity (Hoehn–Yahr) and occurred in the context of reduced arousal ratings of aversive pictures. These findings of blunted startle reactivity add to the literature on emotional changes associated with Parkinson's disease. The basis for this muted reactivity is unknown but may involve an amygdala-based translational defect whereby the results of cognitive appraisal are not appropriately transcoded into somato-motor-arousal responses normally associated with an aversive motivational state. This may arise from faulty dopaminergic gating of the amygdala, resulting in ‘inhibition’ of the amygdala in the manner described by Marowsky et al. (Marowsky A, Yanagawa Y, Obata K, Vogt E. Neuron 2005; 48: 1025–37). More broadly, the findings of muted reactivity to aversive stimuli may reflect a ‘bradylimbic’ affective disturbance in patients with Parkinson's disease. Future studies are needed to address whether the physiologic blunting observed here might be a useful correlate of apathy.
Key Words: amygdala; depression; dopamine; emotion; psychophysiology; startle
Abbreviations: BDI, Beck Depression Inventory; UPDRS, Unified Parkinson's Disease Rating Scale
Received July 11, 2006. Revised September 11, 2006. Accepted September 26, 2006.
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