一次无聊之提升学术英语想法

Memory consolidation reconfigures neural pathways involved in the suppression of emotional memories

 Yunzhe Liu, Wanjun Lin, Chao Liu, Yuejia Luo, Jianhui Wu, Peter J. Bayley & Shaozheng Qin

• Nature Communications 7, Article number: 13375 (2016)

• doi:10.1038/ncomms13375

• Received:06 December 2015

• Accepted:27 September 2016

• Published online:29 November 2016

Abstract

The ability to suppress unwanted emotional memories is crucial for human mental health. Through consolidation over time, emotional memories often become resistant to change. However, how consolidation impacts the effectiveness of emotional memory suppression is still unknown. Using event-related fMRI while concurrently recording skin conductance, we investigated the neurobiological processes underlying the suppression of aversive memories before and after overnight consolidation. Here we report that consolidated aversive memories retain their emotional reactivity and become more resistant to suppression. Suppression of consolidated memories involves higher prefrontal engagement, and less concomitant hippocampal and amygdala disengagement. In parallel, we show a shift away from hippocampal-dependent representational patterns to distributed neocortical representational patterns in the suppression of aversive memories after consolidation. These findings demonstrate rapid changes in emotional memory organization with overnight consolidation, and suggest possible neurobiological bases underlying the resistance to suppression of emotional memories in affective disorders.

Introduction

Our memories for aversive or traumatic events are often vivid and long lasting relative to that of non-aversive or neutral experiences. The enhancement of aversive memory is thought to be due to autonomic reactions to the emotional charge stimulating the encoding and subsequent consolidation of what is referred to as an ‘emotional memory’^1,2. Although emotional memories are enduring, they can, to some extent, be consciously controlled through voluntary suppression in healthy individuals^3,4. A failure to suppress unwanted memories has been linked to symptoms in a number of psychiatric disorders including the ruminative state found in depression and intrusive memories in posttraumatic stress disorder (PTSD)^5,6,7,8. Over time, emotional memories often become more resistant to suppression most likely through a process of consolidation in which sleep is thought to play a vital role^7,9,10. However, it remains unknown how consolidation impacts the effectiveness of voluntary suppression of unwanted emotional memories.

Laboratory studies of the neural basis of memory suppression often use a suppression-induced or motivated forgetting paradigm—the ‘Think/NoThink (TNT)’ procedure^3,4,11, in which inhibitory control of a newly acquired memory is assessed by the compromised ability to recall it at a later time point^3,12. Experiments have shown memory suppression to involve right dorsolateral prefrontal cortex (DLPFC) activation and concomitant reduced hippocampal engagement^11,13, as well as reduced amygdala activity for emotional memories^4,5. In other words, prefrontal inhibitory control over the hippocampal memory and amygdala emotional systems is believed to play a crucial role in voluntary suppression of emotional memories. However, previous studies of memory suppression typically involve materials that are acquired and recalled within minutes or a few hours. In reality, most emotional memories involve events that occurred days, months or years ago. Such memories are expected to be stabilized and assimilated into long-term memory system through consolidation processes^1,14,15.

Many models of memory consolidation suggest that newly acquired memories are initially dependent on the hippocampus and surrounding medial temporal lobe (MTL) structures, and gradually become dependent on a network of cortical regions^1,15,16,17. Critically, newly acquired memories are labile and susceptible to change^11,18,19. Over time they become stabilized in the neocortex through consolidation^14,15. Memory consolidation involves reorganization at both the synaptic and systems levels²⁰. Synaptic consolidation is thought to be complete within hours following learning, and involves the stabilization of synaptic connectivity in local circuits²¹. By contrast, systems consolidation is a more prolonged process and involves gradual reorganization of the brain regions that support long-term memory^1,15. The timecourse of memory consolidation at the systems level appears to be in the order of several years¹⁵. Notably, recent human neuroimaging studies suggest that consolidation can lead to measurable changes over a 24-h period²². Such findings are consistent with the notion that systems consolidation depends at least in part on overnight sleep^7,9. Thus, memories following overnight sleep may undergo notable changes in functional organization between the hippocampus and distributed neocortical regions²². As a result, distinct mechanims may be involved in the suppression of consolidated memories following overnight sleep. However, we know very little about how overnight consolidation impacts brain functional pathways underlying voluntary suppression of emotional memories.

We addressed this question using an event-related functional magnetic resonance imaging (fMRI) memory suppression task coupled with overnight consolidation, which included memory acquisition, TNT and post-scan testing phases (Fig. 1a–c). During the acquisition phase, participants were trained to remember two sets of associations between faces and aversive scenes on two consecutive days, which occurred about 24 h and 30 min before fMRI scanning. During the Think/NoThink phase, participants underwent fMRI while performing the ‘TNT’ task^2,3, in which faces served as cues, with half of the cues learnt 30-min before (that is, newly acquired condition) and the other half learnt 24 h (that is, overnight consolidation condition) before scanning. Skin conductance responses (SCRs) were recorded simultaneously with fMRI scanning to provide an on-line monitoring of physiological reactivity associated with aversive memories. During the post-scan testing phase, participants performed a cued-recall memory test to validate suppression-induced forgetting. Notably, behavioural and physiological data from another independent cohort of 25 participants were used for replication purposes to confirm the stability and robustness of the observed effects of overnight consolidation on suppression of aversive memories. An additional behavioural control experiment with face and neutral stimuli was conducted with another independent 30 participants to investigate the effects of overnight consolidation on suppression of neutral memories.

To further examine the neural representations associated with individual memories before and after overnight consolidation, we implemented a novel analytic approach based on multivariate pattern dissimilarity of item-specific neural activity^23,24,25. This method has been used to identify the representational patterns of neural population codes by means of representational distance matrices^24,26, and provides a unique way to link neuronal activity with representational content of the brain’s memory information processing^19,27,28,29. We show that aversive memories after overnight consolidation become more resistant to suppression, as evidenced by less suppression-induced forgetting and enduring SCR levels. Suppression of consolidated aversive memories, relative to newly acquired ones, appears to involve higher prefrontal inhibitory engagement, but accompanied with less concomitant hippocampal and amygdala disengagement. These effects are paralleled with a shift away from hippocampal-dependent representational patterns to distributed neocortical representational patterns in suppression of aversive memories after overnight consolidation. Altogether, our findings provide converging evidence to support that overnight consolidation assimilates emotional memories into more distributed representational patterns in the neocortex, thus making these memories more resistant to suppression through prefrontal-hippocampal inhibitory pathway.