The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions

doi:10.1016/j.neuroscience.2004.09.054

Neuroscience

Volume 131, Issue 2, 2005, Pages 523-534

https://doi.org/10.1016/j.neuroscience.2004.09.054 Get rights and content

Abstract

We previously found that patients with Parkinson’s disease (PD) were impaired with respect to recognition of fear and disgust in facial expressions. To investigate the neural mechanisms that underlie this impairment, we recorded visual event-related potentials (ERPs) in response to the viewing of fearful facial expressions. Ten normal elderly volunteers and nine patients with PD were studied. Fearful, surprised, and neutral facial expressions were presented randomly for 500 ms each, with a probability of 0.1, 0.1, and 0.8, respectively. The locations of the components of the ERPs were analyzed using a scalp-skull-brain/dipole tracing method. The ERPs elicited in response to the facial stimuli consisted of a negative peak (N1), two positive peaks, and a subsequent slow negative shift. For N1, the equivalent current dipoles were concentrated in the fusiform gyrus, right superior temporal gyrus, parahippocampal gyrus, cingulate cortex, and cerebellum, in normal subjects. In response to the fearful stimulus, dipoles were also generated from the amygdala in seven out of 10 normal subjects. In contrast, in patients with PD, N1 was centered bilaterally in the angular gyrus and supramarginal gyrus, and there was no neuronal activity in the amygdala. After N1, dipoles moved toward the frontal region in normal subjects, whereas they remained in the parietal lobes in patients with PD. These results suggest that neither the amygdala nor the temporal visual-associated cortices are involved in responding to fearful expressions in patients with PD. Corticostriatal connections may be variably affected by a lack of dopamine or by pathological changes in the amygdala. Thus, somatosensory recruitment may overcome the mild cognitive emotional deficits that are present in patients with PD owing to a dysfunction of the amygdala.

Section snippets

Subjects

Ten elderly healthy normal volunteers (range of age: 49–71 years; median: 63.5; all male) and nine patients with PD (range of age: 51–79 years; median: 72; seven males, two females) participated in the study. All patients were treated with medications that are appropriate for patients with PD. The severity of parkinsonian symptoms in all cases was equivalent to 2 or 3 on the Hoehn-Yahr scale (Hoehn and Yahr, 1967). As anxiety causes activation of the amygdala (Masaoka and Homma, 2000), the

Task performance

The normal subjects responded correctly to 98.5±1.24% of the stimuli, whereas the patients with PD responded to 98.9±0.65%. As is evident from the percentage of correct responses and RTs (Table 1), normal subjects and patients with PD performed the task equally well (Mann-Whitney U test, P>0.05). The mean STAI scores for anxiety were 40.2±5.9 in normal subjects and 42.3±11.2 in patients with PD. The mean scores for state anxiety were 40.9±8.6 in normal subjects and 37.6±8.4 in patients with PD.

Discussion

The most important observation in this study was that the ERPs elicited in response to fearful facial expressions were generated within the parietal somatosensory cortex in patients with PD, whereas the equivalent ECDs in normal subjects were located in the amygdala and visual temporal cortex. These findings support our hypothesis that dysfunction of the amygdala in patients with PD causes a change in the neural substrates that are normally used to recognize emotion.

Conclusions

This study revealed that normal subjects and patients with PD use different neural substrates to recognize emotion in facial expressions. The ECDs for component N1 of the ERPs evoked by fearful facial expressions were located in the parietal-associated cortex, in patients with PD. In normal subjects, the dipoles for the same stimulus were generated in the fusiform gyrus, amygdala, parahippocampal gyrus, and superior temporal gyrus, and then moved to the left orbitofrontal gyrus and middle

Acknowledgments

We are grateful to Dr. T. Nagamine (Human Brain Research Center, Kyoto University Graduate School of Medicine) for technical advice, and to Prof. Y. Okamoto (Chiba Institute of Technology), Dr. M. Inoue (Department of Neurology, Showa University School of Medicine), and Prof. Y. Iwamura (Kawasaki University of Medical Welfare) for useful criticism of an earlier version of this manuscript.

This study was supported in part by a Showa University Grant-in-Aid for Innovative Collaborative Research

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The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions

Abstract

Section snippets

Subjects

Task performance

Discussion

Conclusions

Acknowledgments

Neuropsychologia

Trends Cogn Sci

Brain Cogn

Brain Res Cogn Brain Res

Clin Neurophysiol

Trends Neurosci

Neuroscience

Neurosci Lett

Electroencephalogr Clin Neurophysiol

Neurosci Res

Cortex

Neuroimage

Neurosci Lett

Neurosci Res

Brain Res Cogn Brain Res

Brain Res Bull

Int J Psychophysiol

Psychiatry Res

Psychiatry Res

Neuropsychologia

Neuroscience

Brain Res Cogn Brain Res

Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

Nature

Fear and the human amygdala

J Neurosci

Intact recognition of facial emotion in Parkinson’s disease

Neuropsychology

A role for the somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping

J Neurosci

Electrophysiological studies of human face perceptionI. Potentials generated in occipitotemporal cortex by face and non-face stimuli

Cereb Cortex

Anatomical organization of the primate amygdaloid complex