The prelimbic cortex directs attention toward predictive cues during fear learning

Abstract

The prelimbic cortex is argued to promote conditioned fear expression, at odds with appetitive research implicating this region in attentional processing. Consistent with an attentional account, we report that the effect of prelimbic lesions on fear expression depends on the degree of competition between contextual and discrete cues. Further, when competition from contextual cues is low, we found that PL inactivation resulted in animals expressing fear toward irrelevant discrete cues; an effect selective to inactivation during the learning phase and not during retrieval. These data demonstrate that the prelimbic cortex modulates attention toward cues to preferentially direct fear responding on the basis of their predictive value.

Figure 1.

Schematic representations of excitotoxic lesions and cannulas placement for Experiments 1 and 2. Coronal sections are taken from the following points on the anteroposterior plane beginning at top: +4.20, +3.70, +3.20, and +2.70 mm anterior to bregma (Paxinos and Watson 1998). (A) Shaded areas represent the maximum (dark gray) and minimum (black) extent of the lesions for the animals that were included in behavioral analyses for Experiment 1. Damage typically extended from +4.20 to +2.70 mm anterior to bregma. Subjects with significant damage to the adjacent anterior cingulate or infralimbic cortices were excluded from all analyses. (B) Placement of cannulas tips for Experiment 2. All cannulas placements feel between +3.7 and +2.7 mm anterior to bregma. Animals with placements considered outside the boundaries of the PL cortex (Paxinos and Watson 1998), were excluded from all analyses.

Figure 2.

PL lesions only produce a deficit in responding to a CS when there is high competition between contextual and discrete cues. Rates of responding are represented as mean level of observations in which rats spent freezing during CS presentations in the CS test (±SEM). (A) Rats with PL lesions exhibit greater levels of responding to a context when there is high competition between contextual and discrete cues (B) A deficit in learning about the CS is revealed when rats are tested for levels of responding toward the CS outside of the conditioning context (C) Reducing competition between contextual and discrete cues restores the ability of animals with PL lesions to exhibit fear toward a CS.

Figure 3.

PL inactivation during conditioning disrupted subsequent exhibition of the overshadowing effect, while PL inactivation at test was without effect. Rates of responding are represented as suppression ratios with error bars representing the standard error of the mean (A) Animals receiving saline infusions during conditioning exhibited lower levels of fear to stimuli conditioned in compound relative to stimuli individually paired with the outcome, indicative of an overshadowing effect. Animals receiving infusions of the muscimol into the PL cortex failed to demonstrate this difference. (B) Rats receiving either saline or muscimol infusions during the test session demonstrated the overshadowing effect.