Fear conditioning following a unilateral anterior temporal lobectomy: reduced autonomic responding and stimulus contingency knowledge

Acta Neurol Belg. 2010 Mar;110(1):36-48.

Abstract

Animal research demonstrated that during fear conditioning the amygdala plays a central role in forming an association between the conditioned stimulus (CS) and the unconditioned stimulus (US). Lesion studies conducted in patients who underwent a unilateral anterior temporal lobe resection, however; yielded contradictory findings. To date, it remains unclear whether amygdala damage only affects fear-conditioned startle responding or impairs both the latter and fear-conditioned skin conductance responding (SCR). Moreover inconsistency exists regarding the preservation of contingency knowledge in amygdala-damaged patients. In the current study, a differential fear conditioning task was presented to a unilaterally amygdala-damaged patient group and a healthy control group, recording fear-potentiated startle responses along with SCRs. Retrospectively, the valence of the CSs and contingency awareness was assessed. Unlike the control group, unilaterally amygdala-damaged patients showed neither in their SCRs nor in their valence ratings an effect of fear conditioning. The startle data, however, yielded in none of the two test groups fear-conditioned responding. Finally, considerably fewer patients (37.5%) than controls (95%) acquired correct memory of the presented contingency. Based on these findings we concluded that the fear conditioning impairment in amygdala-damaged patients was not restricted to SCRs, but also affected valence ratings and memory of the presented contingency. A broader theory of the amygdala as relevance detector is proposed in order to account for the diverse neurological findings obtained so far.

MeSH terms

  • Analysis of Variance
  • Anterior Temporal Lobectomy / adverse effects*
  • Anterior Temporal Lobectomy / methods
  • Autonomic Nervous System / physiopathology*
  • Awareness / physiology
  • Conditioning, Classical / physiology*
  • Electromyography
  • Epilepsy, Temporal Lobe / surgery
  • Fear*
  • Female
  • Functional Laterality*
  • Galvanic Skin Response / physiology
  • Humans
  • Magnetic Resonance Imaging / methods
  • Male
  • Reflex, Startle / physiology