Lesions of lateral or central amygdala abolish aversive Pavlovian-to-instrumental transfer in rats.

Vincent D Campese,Joseph E Ledoux,Jeanny Kim,Gabriel Lã¡Zaro-Muã±Oz,Lashawn Pena,Christopher K Cain

doi:10.3389/fnbeh.2014.00161

Abstract

Aversive Pavlovian conditioned stimuli (CSs) elicit defensive reactions (e.g., freezing) and motivate instrumental actions like active avoidance (AA). Pavlovian reactions require connections between the lateral (LA) and central (CeA) nuclei of the amygdala, whereas AA depends on LA and basal amygdala (BA). Thus, the neural circuits mediating conditioned reactions and motivation appear to diverge in the amygdala. However, AA is not ideal for studying conditioned motivation, because Pavlovian and instrumental learning are intermixed. Pavlovian-to-instrumental transfer (PIT) allows for the study of conditioned motivation in isolation. PIT refers to the ability of a Pavlovian CS to modulate a separately-trained instrumental action. The role of the amygdala in aversive PIT is unknown. We designed an aversive PIT procedure in rats and tested the effects of LA, BA, and CeA lesions. Rats received Pavlovian tone-shock pairings followed by Sidman shock-avoidance training. PIT was assessed by comparing shuttling rates in the presence and absence of the tone. Tone presentations facilitated instrumental responding. Aversive PIT was abolished by lesions of LA or CeA, but was unaffected by lesions of BA. These results suggest that LA and CeA are essential for aversive conditioned motivation. More specifically, the results are consistent with a model of amygdala processing in which the CS is encoded in the LA and then, via connections to CeA, the motivation to perform the aversive task is enhanced. These findings have implications for understanding the contribution of amygdala circuits to aversive instrumental motivation, but also for the relation of aversive and appetitive behavioral control.

Highlights

In studies of Pavlovian threat conditioning (PTC) a conditioned stimulus (CS; e.g., tone) is paired with an aversive unconditioned stimulus (US; e.g., footshock)
Eight rats from one batch of basal amygdala (BA) lesions had significant bilateral damage to LA, BA, and CeA. It is not clear what caused these excessively large lesions, perhaps an insufficiently insulated electrode. These rats were re-categorized as “amygdala” lesions and data are presented for comparison with the other groups
Direct comparisons between pre- and post-surgical Pavlovian-to-instrumental transfer (PIT) scores agree with the post hoc analyses. These results indicate that Amygdala, LA and CeA lesions impair aversive PIT without affecting baseline USAA performance

Summary

Introduction

In studies of Pavlovian threat conditioning (PTC) a conditioned stimulus (CS; e.g., tone) is paired with an aversive unconditioned stimulus (US; e.g., footshock). PTC depends on connections between the lateral (LA) and central (CeA) nuclei of the amygdala (Jimenez and Maren, 2009). Similar findings have been obtained with escape from fear (or EFF), a related task (Amorapanth et al, 2000). These findings support a model where (1) LA is critical for CS-US learning, (2) intraamygdala connections between LA and CeA mediate Pavlovian reactions, and (3) LA and BA connections mediate non-habitual instrumental responding (Amorapanth et al, 2000; Cain et al, 2013)

Methods

Results

Conclusion