Episodic memory and Pavlovian conditioning: ships passing in the night
Introduction
The ability to remember emotional events can adaptively guide behavior in future situations. Consequently, memory systems are biased to remember experiences encoded around the time of heightened emotional arousal, referred to as the emotional enhancement of memory. This prioritization of emotional memory is adaptive insofar as it helps ensure that we remember people, places, stimuli, situations, and responses associated with important experiences. Research on emotional memory tends to fall into two largely isolated psychological disciplines with characteristically distinct academic traditions: episodic memory and classical (Pavlovian) conditioning. Emotional episodic memory research is generally concerned with explicitly stated knowledge of details surrounding an emotional experience. It is dominated by research on humans, but informed by a history of non-human animal research focused on hippocampal-dependent learning, such as spatial navigation and object recognition. Classical conditioning, on the other hand, describes both a learning process and an experimental procedure by which animals associate neutral stimuli in the environment with meaningful outcomes (e.g. aversive shock or appetitive reward). Neurobiological research on conditioning is predominately focused on the amygdala for its role in learning, storage, and retrieval of threat memories. The goal of this article is to bring into focus the correspondence between these traditionally separated areas of emotional memory research. We briefly describe how ‘emotional memory’ is experimentally defined in episodic memory and conditioning research, describe challenges to studying emotional memory for each field, and discuss how integrating these areas of research can advance our understanding of emotional learning and memory.
Section snippets
Episodic memory and the trouble with isolating the role of emotion
Episodic memory refers to knowledge of the time, place, or other contextual details of an experience [1]. Research on human episodic memory dates back to at least the late nineteenth century [2, 3, 4], and has typically involved testing people’s ability to explicitly recall or recognize a variety of stimuli (words, images, etc.) or the associations between stimuli. Among the most widely replicated findings in episodic memory research is that emotional events are better remembered with more
Pavlovian conditioning and the trouble of isolating individual learning experiences
Conditioning refers to both a learning process and an experimental procedure by which neutral conditional stimuli (CS) acquire the capacity to elicit learned behavioral conditional responses (CR) via association with a biologically salient unconditional stimulus (US). It is traditionally considered an implicit (non-declarative) form of memory mostly unconnected to declarative memory processes [26] (Figure 1). The dominant conditioning paradigm is threat conditioning. Threat conditioning has
Charting the overlap between episodic memory and Pavlovian conditioning
Because human conditioning research is overwhelmingly informed by cue and context conditioning research in rodents, it is generally unconcerned with declarative memory processes. Likewise, because human episodic memory research is generally concerned with higher-order cognitive functions, it is generally unconcerned with putatively reflexive non-declarative memory systems. Indeed, even in the realm of human fear conditioning these forms of memory are typically viewed as operating independently;
Conclusions and future directions
Here we discussed how synthesizing elements of episodic memory and classical conditioning provides unique insight into the mechanisms of emotional memory. A ‘category conditioning’ paradigm allows neutral stimuli to be ‘tagged’ by emotional experiences before, during, or after learning to study the effects on the prioritization into long-term episodic memory that circumvents many of the confounds that have historically affected the field of emotional episodic memory [14••]. At the same time,
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgments
The authors acknowledge funding from NIH R00 MH106719 to J.E.D., and an H2020 Marie Sklodowska-Curie fellowship and a Branco Weiss fellowship - Society in Science to M.C.W.K.
References (68)
Cognitive and neural mechanisms of emotional memory
Trends Cogn Sci
(2001)- et al.
Emerging directions in emotional episodic memory
Front Psychol
(2017) - et al.
Role of amygdala connectivity in the persistence of emotional memories over time: an event-related fMRI investigation
Cerebral Cortex
(2008) - et al.
Neural activity associated with episodic memory for emotional context
Neuropsychologia
(2001) - et al.
Event-related potential correlates of the retrieval of emotional and nonemotional context
J Cogn Neurosci
(2004) - et al.
Retrieved emotional context influences hippocampal involvement during recognition of neutral memories
NeuroImage
(2016) - et al.
The effects of acute stress on episodic memory: A meta-analysis and integrative review
Psychol Bullet
(2017) Issues in the extinction of specific stimulus-outcome associations in Pavlovian conditioning
Behav Processes
(2012)- et al.
Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field
Brain
(2001) - et al.
Event segmentation protects emotional memories from competing experiences encoded close in time
Nat Hum Behav
(2018)
Reward retroactively enhances memory consolidation for related items
Learn Mem
Context and behavioral processes in extinction
Learn Mem
What constitutes an episode in episodic memory?
Psychol Sci
Reconciling reinforcement learning models with behavioral extinction and renewal: implications for addiction, relapse, and problem gambling
Psychol Rev
Memory systems of the brain: a brief history and current perspective
Neurobiol Learn Mem
Episodic memory: from mind to brain
Annual Rev Psychol
Memory: a contribution to experimental psychology
Ann Neurosci
A brief history of memory research
The Oxford Handbook of Memory
Cognitive neuroscience of emotional memory
Nat Rev Neurosci
Oversimplification in the study of emotional memory
J Int Neuropsychol Soc
fMRI studies of successful emotional memory encoding: a quantitative meta-analysis
Neuropsychologia
Paired-associate learning as a function of arousal and interpolated interval
J Exp Psychol
How arousal modulates memory: disentangling the effects of attention and retention
Cogn, Affect, Behav Neurosci
The slow forgetting of emotional episodic memories: an emotional binding account
Trends Cogn Sci
Enhanced emotional memory: cognitive and neural mechanisms
Curr Direct Psychol Sci
Mechanisms of emotional arousal and lasting declarative memory
Trends Neurosci
The role of attention and relatedness in emotionally enhanced memory
Emotion
Task and content modulate amygdala-hippocampal connectivity in emotional retrieval
Neuron
The amygdala modulates the consolidation of memories of emotionally arousing experiences
Ann Rev Neurosci
Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding
Learn Mem
Stress as a mnemonic filter: Interactions between medial temporal lobe encoding processes and post‐encoding stress
Hippocampus
Emotional brain states carry over and enhance future memory formation
Nat Neurosci
Structure and function of declarative and nondeclarative memory systems
Proc Nat Acad Sci U S A
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