Neural substrates of explicit and implicit fear memory

Abstract

Distinct aspects of our fearful experiences appear to be mediated by separate explicit and implicit memory processes. To identify brain regions that support these separate memory processes, we measured contingency awareness, conditional fear expression, and functional magnetic resonance imaging signal during a Pavlovian fear conditioning procedure in which tones that predicted an aversive event were presented at supra and sub-threshold volumes. Contingency awareness developed in conjunction with learning-related hippocampal and parahippocampal activity on perceived conditioning trials only. In contrast, conditional fear and differential amygdala activity developed on both perceived and unperceived trials, regardless of whether contingency awareness was expressed. These findings demonstrate the distinct roles of these brain regions in explicit and implicit fear memory processes.

Figure 1

UCS expectancy & SCR data. a) Learning-related changes in UCS expectancy were demonstrated on perceived trials only. Larger responses were produced during the CS+ relative to the CS− on perceived, but not unperceived trials. b) In contrast, learning-related SCRs were demonstrated on both perceived and unperceived trials. The CS+ produced larger SCRs than the CS− on both perceived and unperceived conditioning trials. Asterisk indicates significant difference. Error bars represent standard error of the mean.

Figure 2

Functional MRI data. Learning-related changes in the area under the hemodynamic response curve (AUC) were observed within the hippocampus on perceived trials only. Larger responses were observed during perceived CS+ relative to perceived CS− presentations, while responses to the CS+ and CS− did not differ on unperceived trials. Asterisk indicates significant difference. Error bars represent standard error of the mean.

Figure 3

Functional MRI data. Learning-related changes in the area under the hemodynamic response curve (AUC) were observed within the amygdala during both perceived and unperceived trials. The AUC was larger during the CS+ than CS− on both perceived and unperceived trials. Asterisk indicates significant difference. Error bars represent standard error of the mean.