Functional MRI of human amygdala activity during Pavlovian fear conditioning: Stimulus processing versus response expression.

Abstract

Although laboratory animal studies have shown that the amygdala plays multiple roles in conditional fear, less is known about the human amygdala. Human subjects were trained in a Pavlovian fear conditioning paradigm during functional magnetic resonance imaging (fMRI). Brain activity maps correlated with reference waveforms representing the temporal pattern of visual conditional stimuli (CSs) and subject-derived autonomic responses were compared. Subjects receiving paired CS-shock presentations showed greater amygdala activity than subjects receiving unpaired CS-shock presentations when their brain activity was correlated with a waveform generated from their behavioral responses. Stimulusbased waveforms revealed learning differences in the visual cortex, but not in the amygdala. These data support the view that the amygdala is important for the expression of learned behavioral responses during Pavlovian fear conditioning.

Human amygdala activity during the expression of fear responses.

“…The unilateral findings in both experiments were largely consistent with previous neuroimaging studies of fear conditioning (Büchel et al, 1998;Cheng et al, 2003;LaBar et al, 1998). However, left amygdala activity during fear learning has also been reported (Morris, Ohman, & Dolan, 1998;Phelps et al, 2001).…”

“…Consistent with this view, one study from our laboratory (Cheng at al., 2003), conducted with an analytical approach emphasizing sensitivity to the response-generating functions of the amygdala, found significant amygdala activity, whereas another study (Knight, Cheng, Smith, Stein, & Helmstetter, 2004a) involving a more traditional analysis technique and focusing on stimulusprocessing properties of the amygdala, failed to detect differential amygdala activity. The current article revisited this data set that failed to show significant amygdala activity (Knight et al, 2004a) in order to determine whether activity within this region can be better predicted by an analytical approach emphasizing response expression.…”

“…More complex conditioning procedures designed to retard acquisition may be able to address response-related amygdala activity during later training trials. Cheng et al (2003) was an initial attempt at using autonomic fear responses to guide functional imaging analyses. The current analysis addressed specific concerns of this study, which include limitations that accompany a block design, correlational findings, and a between-groups analysis.…”

“…Given that SCR topography is remarkably similar to the pattern of responding observed in the amygdala during fear conditioning, it is not surprising that several different laboratories (Büchel et al, 1998;Cheng, Knight, Smith, Stein, & Helmstetter, 2003;LaBar et al, 1998;Phelps et al, 2001) have demonstrated a correlation between these two measures. These findings support the possibility that human amygdala activity may not exclusively reflect the learning of stimulus associations but may also be involved in the expression of autonomic conditional fear.…”

Differential fear conditioning in Asperger's syndrome: Implications for an amygdala theory of autism

“…First, as Bernier and colleagues point out, such studies contribute to our understanding of the neuropathology underlying this spectrum of disorders. Extensive animal (see LeDoux, 1994LeDoux, , 1995LeDoux, , 1998LeDoux, , 2000 for detailed reviews) and human (Bechara, Tranel, Damasio, Adolphs, Rockland & Damasio, 1995;Büchel, Morris, Dolan & Friston, 1998;Büchel, Dolan, Armony & Friston, 1999;Cheng, Knight, Stein & Smith, 2003;Knight, Smith, Cheng & Stein, 2004;LaBar, LeDoux, Spencer & Phelps, 1995;LaBar, Gatenby, Gore, LeDoux & Phelps, 1998;Morris, Őhman & Dolan, 1997;Morris, Friston & Dolan, 1997Phelps, LaBar, Anderson, O'Connor, Fulbright & Spencer, 1998) research has demonstrated that the associative learning in fear conditioning paradigms is mediated by the amygdala, a limbic structure which has attracted increasing attention in relation to ASD in recent years. Although several lines of research have implicated the amygdala in the pathology underlying this disorder (e.g.…”