Fear processing and social networking in the absence of a functional amygdala.
BACKGROUND
The human amygdala plays a crucial role in processing social signals, such as face expressions, particularly fearful ones, and facilitates responses to them in face-sensitive cortical regions. This contributes to social competence and individual amygdala size correlates with that of social networks. While rare patients with focal bilateral amygdala lesion typically show impaired recognition of fearful faces, this deficit is variable, and an intriguing possibility is that other brain regions can compensate to support fear and social signal processing.


METHODS
To investigate the brain's functional compensation of selective bilateral amygdala damage, we performed a series of behavioral, psychophysiological, and functional magnetic resonance imaging experiments in two adult female monozygotic twins (patient 1 and patient 2) with equivalent, extensive bilateral amygdala pathology as a sequela of lipoid proteinosis due to Urbach-Wiethe disease.


RESULTS
Patient 1, but not patient 2, showed preserved recognition of fearful faces, intact modulation of acoustic startle responses by fear-eliciting scenes, and a normal-sized social network. Functional magnetic resonance imaging revealed that patient 1 showed potentiated responses to fearful faces in her left premotor cortex face area and bilaterally in the inferior parietal lobule.


CONCLUSIONS
The premotor cortex face area and inferior parietal lobule are both implicated in the cortical mirror-neuron system, which mediates learning of observed actions and may thereby promote both imitation and empathy. Taken together, our findings suggest that despite the pre-eminent role of the amygdala in processing social information, the cortical mirror-neuron system may sometimes adaptively compensate for its pathology.
Department of Psychiatry, University of Bonn, Germany.
Benjamin
B
Becker
Yoan
Y
Mihov
Dirk
D
Scheele
Keith M
KM
Kendrick
Justin S
JS
Feinstein
Andreas
A
Matusch
Merve
M
Aydin
Harald
H
Reich
Horst
H
Urbach
Ana-Maria
AM
Oros-Peusquens
Nadim J
NJ
Shah
Wolfram S
WS
Kunz
Thomas E
TE
Schlaepfer
Karl
K
Zilles
Wolfgang
W
Maier
René
R
Hurlemann
D000293:Adolescent; D000679:Amygdala / Q000503:physiopathology*; D001921:Brain / Q000503:physiopathology*; D001931:Brain Mapping / Q000379:methods; D017352:Echo-Planar Imaging / Q000379:methods; D005149:Facial Expression; D005239:Fear / Q000523:psychology*; D005260:Female; D006801:Humans; D008065:Lipoid Proteinosis of Urbach and Wiethe / Q000503:physiopathology*; D008279:Magnetic Resonance Imaging / Q000379:methods; D008606:Mental Processes; D021641:Recognition, Psychology; D013216:Reflex, Startle; D012919:Social Behavior; D014430:Twins, Monozygotic / Q000523:psychology