Startling facts about emotion in Parkinson's disease: blunted reactivity to aversive stimuli

• Published in: Brain (London, England : 1878) England : 1878), 2006-12, Vol.129 (12), p.3356-3365
• Main Authors: Bowers, Dawn, Miller, Kimberly, Mikos, Ania, Kirsch-Darrow, Lindsey, Springer, Utaka, Fernandez, Hubert, Foote, Kelly, Okun, Michael
• Format: Article
• Language: English
• Subjects: amygdala; Anti-Anxiety Agents - therapeutic use; Antidepressive Agents - therapeutic use; Antiparkinson Agents - therapeutic use; Arousal - physiology; Biological and medical sciences; Blinking - physiology; Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases; depression; Depression - physiopathology; Depression - psychology; dopamine; Dopamine Agents - therapeutic use; emotion; Emotions - physiology; Female; Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy; Humans; Levodopa - therapeutic use; Male; Medical sciences; Middle Aged; Nervous system (semeiology, syndromes); Neurology; Parkinson Disease - physiopathology; Parkinson Disease - psychology; Photic Stimulation - methods; psychophysiology; Reaction Time; Reflex, Startle - physiology; Severity of Illness Index; startle
• ISSN: 0006-8950; 1460-2156
• DOI: 10.1093/brain/awl301

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