Context-dependent extinction of threat memories: influences of healthy aging

Simone Battaglia,Sara Garofalo,Giuseppe Di Pellegrino

doi:10.1038/s41598-018-31000-9

Simone Battaglia, Sara Garofalo + Show 1 more

Open Access

https://doi.org/10.1038/s41598-018-31000-9

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Abstract

Although a substantial progress has been made in recent years on understanding the processes mediating extinction of learned threat, little is known about the context-dependent extinction of threat memories in elderly individuals. We used a 2-day differential threat conditioning and extinction procedure to determine whether young and older adults differed in the contextual recall of conditioned responses after extinction. On Day 1, conditioned stimuli were paired with an aversive electric shock in a ‘danger’ context and then extinguished in a different ‘safe’ context. On Day 2, the extinguished stimulus was presented to assess extinction recall (safe context), and threat renewal (danger context). Physiological and verbal report measures of threat conditioning were collected throughout the experiment. Skin conductance response (SCR data revealed no significant differences between age groups during acquisition and extinction of threat conditioning on Day 1. On Day 2, however, older adults showed impaired recall of extinction memory, with increased SCR to the extinguished stimulus in the ‘safe’ context, and reduced ability to process context properly. In addition, there were no age group differences in fear ratings and contingency awareness, thus revealing that aging selectively impairs extinction memories as indexed by autonomic responses. These results reveal that aging affects the capacity to use context to modulate learned responses to threat, possibly due to changes in brain structures that enable context-dependent behaviour and are preferentially vulnerable during aging.

Highlights

Extinction of threat memories is a phenomenon that allows animals and humans to adapt their behaviour to a changing environment
We presented visual conditioned stimulus (CS) embedded within pictures of two distinct rooms, such that, on Day 1, threat acquisition and extinction training were performed in contexts A and B, respectively
A 2 × 2 repeated measure ANOVA was performed on skin conductance response (SCR), with Group as a between-subject factor, and Stimulus (CS+/CS−), as a within-subject factor

Summary

Introduction

Extinction of threat memories is a phenomenon that allows animals and humans to adapt their behaviour to a changing environment. There is converging evidence from animal[5,6,7,8] and human[9,10] studies that the mechanisms supporting extinction entail new learning (i.e., CS-no US) that competes, and temporarily interferes, with the expression of the original conditioning trace. To test for context-dependent recall of extinction memory in aging, we used a 2-day differential threat conditioning and extinction procedure, modified from that previously described by Milad and colleagues[39,41] (see Fig. 1) This protocol incorporates a temporal delay (24 hr) between extinction training and subsequent probing of extinction and threat memories, providing a more ecological test of long-term extinction memories in young and older adults. Physiological (skin conductance) and verbal report measures of threat conditioning were collected throughout the experiment

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