Differential involvement of the basolateral amygdala and mediodorsal thalamus in instrumental action selection

Abstract

Although it has been shown that the basolateral amygdala (BLA) and the mediodorsal thalamus (MD) are critical for goal-directed instrumental performance, much remains unknown about the respective contributions of these structures to action selection. The current study assessed the effects of post-training BLA and MD lesions on several tests of instrumental action selection. We found that MD damage disrupted the influence of pavlovian cues over action selection but left intact rats' ability to select actions based on either the expected value or the discriminative stimulus properties of the outcome. In contrast, BLA lesions impaired performance on all three tests of action selection. Because both lesion types disrupted the influence of cues that signal reward over instrumental performance, we then investigated the involvement of these structures in pavlovian contingency learning using a task in which the predictive status of one of two cues is degraded by delivering its outcome noncontingently during the intertrial interval. As expected, the sham group selectively suppressed their conditioned approach performance to the cue that no longer signaled its outcome but continued to respond to the control stimulus. In contrast, both lesioned groups were impaired on this task. Interestingly, whereas the MD group displayed a nonspecific reduction in responding to both cues, the BLA group continued to show high levels of responding to both cues as if their performance was completely insensitive to this contingency manipulation. These findings demonstrate that the BLA and MD make important yet distinct contributions to instrumental action selection.

Figure 1.

Histological results. A–F, Photomicrographs of the MD (A, C, E) and BLA (B, D, F). Representative excitotoxic lesions are shown at low (4×) (A, B) and high (10×) (C, D) magnification. Representative sham lesions are shown at high magnification only (E, F). CL, Centrolateral thalamic nucleus; CeN, central amygdala. G, F, Schematic representation of the minimum (black outline) and maximum (gray shading) extent of damage resulting from MD (G) and BLA (H) lesions. (Adapted from Paxinos and Watson, 1998.)

Figure 2.

Effects of MD and BLA lesions on instrumental action selection based on outcome value. Mean lever presses per minute (±SEM) over the 5 min choice extinction test. The data are presented separately for the action paired with the devalued outcome (devalued) and the action paired with the other outcome (nondevalued).

Figure 3.

Effects of MD and BLA lesions on cue-guided action selection. Mean lever presses per minute (+SEM) during the precue period (baseline), the cue that signaled the same outcome as the action (Same) and the cue that signaled the outcome paired with the other action (Different).

Figure 4.

Effects of MD and BLA lesions on outcome-guided action selection. Mean lever presses per minute (+SEM) during the preoutcome period (baseline), after the delivery of the outcome that was paired with that action (Same) and after the delivery of the outcome was paired with the other action (Different).

Figure 5.

Effects of MD and BLA lesions on pavlovian contingency degradation learning. The left panel shows the mean number of seconds spent in the food magazine (±SEM) during the precue period (baseline), the cue that was paired with the noncontingently delivered outcome (degraded), and the cue that was paired with the other outcome (nondegraded). For convenience, these data are presented in the right panel as a difference score (stimulus − baseline).