Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats

Abstract

Lesions of the basolateral amygdala (BLA) have long been associated with abnormalities of taste-related behaviors and with failure in a variety of taste- and odor-related learning paradigms, including taste-potentiated odor aversion, conditioned taste preference, and conditioned taste aversion. Still, the general role of the amygdala in chemosensory learning remains somewhat controversial. In particular, it has been suggested that the amygdala may not be involved in a form of chemosensory learning that has recently received a substantial amount of study-socially transmitted food preference (STFP). Here, we provide evidence for this involvement by pharmacologically inactivating the basolateral amygdala bilaterally during STFP training. The same inactivation sites that impaired taste aversion learning eliminated the normally conditioned preference for a food smelled on a conspecific's breath. Impairments of learned preference persisted even in testing sessions in which BLA was not inactivated, and learning was normal when the BLA was inactivated only during testing sessions; thus, the impairment was a true acquisition deficit. In conjunction with previous results from other paradigms, therefore, our data suggest that the amygdala is vital for learning procedures involving pairings of potent and arbitrary chemosensory stimuli.

Figure 1.

BLA inactivation impairs STFP. The y-axis shows milligrams of each diet consumed. (A) For animals with the BLA inactivated (left bars), the demonstrated diets (white bar) were not preferred over undemonstrated diets (gray bar). Rats with an intact BLA (right bars), meanwhile, clearly show a preference for the demonstrated diet, which made up almost 80% of their total consumption during T1. *P < 0.02. (B) STFP learning was maintained in saline-infused rats. As on T1, on T7 saline-infused rats strongly preferred the demonstrated over the undemonstrated diet. Animals in the muscimol-infused group, meanwhile, ingested equal amounts of the demonstrated and undemonstrated diets. *P < 0.005. In this and all later figures, error bars = SEM.

Figure 2.

BLA is necessary for acquisition but not expression of STFP. The y-axis shows milligrams of each diet consumed. During T1, rats for which the BLA was inactivated during training (left bars) consumed equal amounts of the demonstrated (white bar) and undemonstrated (gray bar) diets; i.e., they failed to show learning even when tested with an intact BLA. Rats trained with an intact BLA (saline-infused, right bars) showed a strong preference for the demonstrated diet, despite being tested with inactivated BLA. *P < 0.001.

Figure 3.

Behaviors used to measure CTA for Experiment 3. (A) Gapes are a yawn-like opening of the rat’s mouth, in which the teeth are exposed and the jaw flexed up and down. (B) Head-shakes were recorded when the snout was moved quickly from one side of the body to the other. (C) Lateral arm-flails were high-frequency movements during which the rat’s forepaws were flung laterally and then brought together under the snout.

Figure 4.

BLA inactivation impairs CTA learning using IOC taste delivery. The y-axis shows the number of aversive responses (i.e., sum of gapes, head shakes, and limb flails) produced in response to IOC-delivered sucrose during testing sessions. Rats that received BLA saline infusions during training (black bar) showed roughly twice as many aversive responses as experimental animals that received BLA muscimol infusions during training (white bar). Wilcoxon*P < 0.02.

Figure 5.

Inactivation of BLA does not impair CTA in the one-bottle test. The y-axis shows the difference between the amount of sucrose consumed during the session just before LiCl injection (most rats consumed the full 10 mL available) and the testing session. The reduction in consumption for each group is significantly greater than zero, demonstrating successful learning. The effect of BLA inactivation on this learning, meanwhile, was not significant, demonstrating a lack of amygdalar involvement in this particular form of CTA.

Figure 6.

The site vital for STFP acquisition can be localized to the BLA. (A) Sample histology, showing the placement of the cannula. The vertical lesions show the cannula tract, leading down toward the BLA. (B) A random subset (n = 31) of cannula tip sites are shown superimposed on a schematic representation of the rats’ brain in the A-P plane (−2.80 mm from Bregma) of cannula implantation (Reprinted with permission from Elsevier © 1997, Paxinos and Watson 1997). (Gray shading, extent of left BLA).