Activity in the human amygdala corresponds to early, rather than late period autonomic responses to a signal for shock

Abstract

Laboratory animal and human subject studies report that the amygdala is a critical brain structure that supports the acquisition and expression of conditional fear. Recent functional neuroimaging studies in humans have reported that activity in this region is closely related to the behavioral expression of conditional skin conductance responses (SCR). However, SCR waveforms following conditional stimulus (CS) presentation contain both early period and late period responses that may differ with respect to underlying central processes. It is not known whether amygdala activity corresponds to the expression of early conditional responses (CRs) that occur shortly following CS onset or late CRs that closely precede UCS onset. The present study used event-related functional magnetic resonance imaging and concurrent skin conductance measurements to determine whether amygdala activity is more closely related to the expression of early or late period CRs. Increased amygdala activity was detected during the formation of early, but not late period CRs. Additionally, this pattern of amygdala activity did not dissipate, but persisted into late stages of the experiment. These findings are consistent with the idea that amygdala responding is critically involved in the generation of CRs formed shortly following CS onset.

Figure 1.

Behavioral data across 12 CS+ and 12 CS− trials. (A) Averaged explicit responses to CS+ and CS− trials. Subjects demonstrated rapid acquisition of the CS–UCS relationship. (B) Averaged SCR to CS+ and CS− trials. CS+ trials elicited significantly higher magnitude SCRs relative to CS− trials, demonstrating implicit discrimination in subjects.

Figure 2.

Imaging and behavioral data for early and late period CRs during the first half of the experiment. (Top) Coronal close-up of a contrast between early and late CRs revealed a cluster of activation in the right amygdala (Talairach coordinates: 13 −7 −12; 172 μL). (A) Increased amygdala activity was detected during early period CRs. (B) Decreased amygdala activity was detected during late period CRs. (C) Averaged SCR waveform during trials that elicited early CRs. (D) Averaged SCR waveform during trials that elicited late CRs.

Figure 3.

Comparison of amygdala responding during the first and second half of the experiment. White bars indicate amygdala activity during trials that elicited early CRs, while black bars denote amygdala responding during late CRs.

Figure 4.

A similar topography of conditional SCRs was observed between the first and second half of the study. Solid lines signify responding during the first half of the study, and dotted lines refer to the second half of the study. Increased amygdala responding was only detected during early period responses (shaded area of left graph) but not during late period responses (shaded area of right graph).