Perceiving threat in the face of safety: excitation and inhibition of conditioned fear in human visual cortex

Abstract

Previous findings have established that cortical sensory systems exhibit experience-dependent biases toward stimuli consistently associated with threat. It remains unclear whether safety cues also facilitate perceptual engagement or how competition between learned threat and safety cues is resolved within visual cortex. Here, we used classical discrimination conditioning with simple luminance modulated visual stimuli that predicted the presence or absence of an aversive sound to examine visuocortical competition between features signaling threat versus safety. We tracked steady-state visual evoked potentials to label distinct visual cortical responses in humans to conditioned and control stimuli. Trial-by-trial expectancy ratings collected online confirmed that participants discriminated between threat and safety cues. Conditioning was associated with heightened activation of the extended visual cortex in response to the threat, but not the safety, stimulus. Cortical facilitation for the threatening stimulus was selective and not decreased by simultaneously presenting safe and associatively novel cues. Our findings shed light on the sensory brain dynamics associated with experience-dependent acquisition of perceptual biases for danger and safety signals.

Figure 1.

A depicts the basic experimental structure and number of trials included in each of the four phases. Data from the extinction block are not presented in this study because it did not relate to the main questions of interest. A schematic of AX+ and BX− trial types in the conditioning phase of the experiment is shown in B. Note that the A+ stimulus (45° clockwise grating) was paired with the aversive sound on 100% of the trials, whereas the B− stimulus (45° anticlockwise grating) was never paired with the aversive sound. The visual stimuli were flickered at two distinct frequencies (14 and 17.5 Hz) with flicker rate assignment for each hemifield being counterbalanced across participants.

Figure 2.

Online trial-by-trial ratings of AX+ (A) and BX− (B) conditioned cues, before CS–UCS pairing (Pre) and during eight successive bins collected during the conditioning phase (each bin represents an average of 2 trials). The y-axis scale represents the horizontal dimension of the display monitor. The dashed gray line represents participants' uncertainty, with higher values indicating greater UCS expectancy and lower values indicating lower expectancy. Error bars depict SEM.

Figure 3.

The Fourier frequency spectrum for Electrical Geodesics sensor 120, averaging across all subjects (n = 21) and experimental blocks. The grand average scalp topography of ssVEP amplitude to the conditional visual stimuli, collapsed across tagging frequencies.

Figure 4.

Means and scalp topographies (mapped with spherical spline interpolation) of ssVEP amplitude during threat cue conditioning, shown separately for the threat cue (A+) paired with the UCS on 100% of the conditioning trials and the background stimulus (X) paired with the UCS on 50% of the conditioning trials. Error bars depict SEM.

Figure 5.

Means and scalp topographies (mapped with spherical spline interpolation) of ssVEP amplitudes evoked by the conditioned threat stimulus and a neutral background cue (conditioning phase, left) and that evoked by the threat and safety cues (transfer phase, right). Error bars depict SEM.