Acquired fears reflected in cortical sensory processing: a review of electrophysiological studies of human classical conditioning

Abstract

The capacity to associate neutral stimuli with affective value is an important survival strategy that can be accomplished by cell assemblies obeying Hebbian learning principles. In the neuroscience laboratory, classical fear conditioning has been extensively used as a model to study learning-related changes in neural structure and function. Here, we review the effects of classical fear conditioning on electromagnetic brain activity in humans, focusing on how sensory systems adapt to changing fear-related contingencies. By considering spatiotemporal patterns of mass neuronal activity, we illustrate a range of cortical changes related to a retuning of neuronal sensitivity to amplify signals consistent with fear-associated stimuli at the cost of other sensory information. Putative mechanisms that may underlie fear-associated plasticity at the level of the sensory cortices are briefly considered, and several avenues for future work are outlined.

Figure 1

An illustration summarizing effects related to an enhancement of CS+ (vs. CS−) responses in sensory regions, gathered from studies that employed transient presentations of the CS cues. The x-axis depicts time from CS-onset and the width of the bars depicts the approximate temporal window of significant effects, as described in the published studies. Black bars depict visual CSs and white bars depict auditory CSs. The asterisk notes an example of a response reversal (i.e., CS− eliciting a greater response than the CS+).

Figure 2

ERP responses to the CS+ (dashed, red line) and CS− (dashed, blue line) experimental conditions averaged across 18 participants, after 160 trials of differential conditioning. Note the amplitude enhancement associated with CS+ processing, beginning with the C1 component, and continuing for the P1 and late positive potential (LPP). Data are taken from Stolarova et al. (2006).

Figure 3

Example of an evoked oscillatory response, elicited by flickering visual stimuli, brightness-modulated at a fixed rate of 10 cycles/second. The resulting scalp-recorded waveform is referred to as steady-state visual evoked potential and represents primarily activity from early sensory areas that are repeatedly engaged by the same stimulus.

Figure 4

On the right, mean amplitudes (n=20) across significant source clusters in occipito-parietal regions. ssVEF amplitude is greater for the CS+ than the CS− in a late temporal window, that precedes US onset. Left panel depicts the distribution of correlation coefficients for the relationship between heart rate change (CS+ acceleration) and increased cortical activation for the CS+. Redrawn from data in Moratti et al., 2006. Bars depict SEM.

Figure 5

The evolutionary spectrum of visual electrocortical responses during classical conditioning. Graphs show a grand mean (n=23) sequence of time-frequency representations of visual responses to the CS+ (top) and CS− (bottom) during 4 stages of classical conditioning, derived using a Morlet wavelet transform (redrawn from data in Keil et al., 2007 and Stolarova et al., 2006). Visible spectral events include an early response in the lower gamma band range (around 80–120 ms at 20–35 Hz), in response to the CS; late high-frequency gamma response to the US onset (at 600 ms post-CS and above 40 Hz); pronounced lower band reduction in response to the US (starting at 400 ms). Note the increase of the early gamma band response during acquisition for the CS+, but not the CS− (white dashed box, top, acquisition 2).