Conditioning method dramatically alters the role of amygdala in taste aversion learning

Abstract

Although an important role for the amygdala in taste aversion learning has been suggested by work in a number of laboratories, results have been inconsistent and interpretations varied. The present series of studies reevaluated the role of the amygdala in taste aversion learning by examining the extent to which conditioning methods, testing methods and lesioning methods, influence whether amygdala lesions dramatically affect conditioned taste aversion (CTA) learning. Results indicated that when animals are conditioned with an intraoral (I/O) taste presentation, lesions of amygdala eliminate evidence of conditioning whether animals are tested intraorally or with a two-bottle solution presentation. Dramatic effects of amygdala lesions on CTA learning were seen whether lesions were made electrolytically or using an excitotoxin. In contrast, when animals were conditioned using bottle presentation of the taste, electrolytic lesions attenuated CTAs but did not eliminate them, and excitotoxic lesions had no effect. These results are consistent with the hypothesis that neural structures critical for CTA learning may differ depending on the extent to which the method of conditioned stimulus delivery incorporates a response component.

Figure 1

Schematic illustration of different methods used to establish a CTA. Rats are either infused intraorally with a CS taste solution followed by injection with toxic drug, such as LiCl (top), or are allowed to drink the CS taste solution from a bottle followed by the same drug (bottom).

Figure 2

Mean rejection latency (±s.e.) of SHAM and electrolytically lesioned animals during I/O saccharin infusion at the time of testing. Saccharin had either been paired (hatched bars) or unpaired (solid bars) with LiCl using I/O conditioning. (**) P < 0.01 relative to unpaired controls (experiment 1).

Figure 3

(top) Mean (±s.e.) preference ratios for SHAm and electrolytically lesioned animals following 12-hr two-bottle test between saccharin and water. Saccharin had either been paired (hatched bars) or unpaired (solid bars) with LiCl using I/O conditioning. (Bottom) Mean (±s.e.) absolute solution intake of water (solid bars) and saccharin (hatched bars) during the same test. (*) P < 0.01 relative to unpaired controls; (#) P < 0.01 relative to water intake in SHAM–Paired controls (experiment 1).

Figure 4

(Top) Mean (± s.e.) preference ratios for SHAM and electrolytically lesioned animals following 12-hr two-bottle test between sacharin and water. Saccharin had either been paired (hatched bars) or unpaired (solid bars) with LiCl using bottle conditioning. (Bottom) Mean (±s.e.) absolute solution intake of water (solid bars) and saccharin (hatched bars) during the same test. (*) P < 0.01 relative to unpaired controls; (#) P < 0.01 relative to water intake in SHAM–Paired controls (experiment 2).

Figure 5

Serial reconstructions of electrolytic amygdala lesions in the transverse plane. (Left) The extent of the lesions in experiment 1, in which animals were conditioned intraorally. (Right) The extent of the lesions in experiment 2, in which rats were conditioned with a bottle. The lightly and darkly shaded regions correspond to the largest and smallest lesions, respectively.

Figure 6

Mean rejection latency (±s.e.) of SHAM and excitotoxically lesioned animals during I/O saccharin infusion at the time of testing. Saccharin had either been paired (P) or unpaired (UnP) with LiCl using I/O conditioning. (*) P < 0.01 relative to lesioned groups (experiment 3a).

Figure 7

(Top) Mean (±s.e.) preference ratios for SHAM and excitotoxically lesioned animals following 12-hr two-bottle test between saccharin and water. Saccharin had either been paired (P) or unpaired (UnP) with LiCl using bottle conditioning. (Bottom) Mean (±s.e.) absolute solution intake of water (solid bars) and saccharin (hatched bars) during the same test. (**) P < 0.01 relative to unpaired controls; (#) P < 0.01 relative to water intake in SHAM–Paired controls (experiment 3b).

Figure 8

Serial reconstructions of excitotoxic amygdala lesions in the transverse plane (experiment 3). (Left) Lesions in experiment 3a in which rats were conditioned with the I/O method. (Right) Lesions in experiment 3b in which rats were conditioned using a bottle. The lightly and darkly shaded regions correspond to the largest and smallest lesions, respectively.

Figure 9

Mean rejection latency (±s.e.) of SHAM and excitotoxically lesioned animals during I/O saccharin infusion at the time of testing. Saccharin had either been paired (P) or unpaired (UnP) with LiCl using I/O conditioning under conditions of fluid deprivation. (**) P < 0.01 relative to lesioned groups (experiment 4).