Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys

Abstract

Aspiration lesions of the amygdala were found previously to produce a severe impairment in visual discrimination learning for auditory secondary reinforcement in rhesus monkeys (Gaffan and Harrison, 1987). To determine whether excitotoxic amygdala lesions would also produce this effect, we trained four naive rhesus monkeys on the same task. The monkeys were required to learn 40 new visual discrimination problems per session in a situation in which visual choices were guided by an auditory secondary reinforcer that had been previously associated with food reward. Bilateral excitotoxic lesions of the amygdala had no effect on the rate of learning visual discrimination problems for auditory secondary reinforcement. We also tested the amygdalectomized monkeys on a reinforcer devaluation task and compared their performance with a group of three normal monkeys. The monkeys first learned to discriminate 60 pairs of objects, baited with two different food rewards. Each of the food rewards was then devalued by selective satiation in two separate experimental sessions. Normal controls tended to avoid displacing objects that covered the devalued food to a significantly greater degree than did the amygdalectomized monkeys, indicating that the excitotoxic amygdala damage interfered with reinforcer devaluation effects. Our results are consistent with the idea that the amygdala is necessary for learning the association between stimuli and the value of particular food rewards; however, the amygdala is not necessary for maintaining the value of secondary reinforcers, once they have been learned.

Fig. 1.

Coronal sections showing the intended lesion (middle column) and the actual extent of damage in four monkeys, A1 and A4 (left column) and A2 and A3 (right column), that received injections of ibotenic acid into the amygdala. Numerals indicate the distance in millimeters from the interaural plane.

Fig. 2.

Photomicrographs of Nissl-stained coronal sections approximately +16 mm from the interaural plane. A, Section through the left amygdala in monkey A4. B, Section through the left amygdala in an intact monkey. Note virtually complete cell loss in the amygdala of the operated monkey (A), with relative preservation of the underlying entorhinal cortex.

Fig. 3.

Photomicrographs of Nissl-stained coronal sections through the amygdala lesion in monkey A4. Top,middle, and bottom sections represent the left and right amygdala at approximately +18, +16, and +14 mm from the interaural plane, respectively.

Fig. 4.

Within-problem learning curves on visual discrimination for auditory secondary reinforcement (Experiment 1) before (PRE-OP) and after (POST-OP) excitotoxic amygdala lesions. Average percent error is shown for the first four trials of new problems (see Table 1).

Fig. 5.

Group mean difference scores, a measure of the effect on choices of objects of reinforcer devaluation (Experiment 2).CONTROL, Unoperated control monkeys (n = 3); AMYGDALA LESION, monkeys with selective, excitotoxic lesions of the amygdala (n = 4). Vertical lines represent the range of scores of individual monkeys.