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Rethinking the Definition of Episodic Memory

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Abstract

The definition of episodic memory, as proposed by Tulving, includes a requirement of conscious recall. As we are unable to assess this aspect of memory in nonhuman animals, many researchers have referred to demonstrations of what would otherwise be considered episodic memory as "episodic-like memory." Here the definition of episodic memory is reconsidered based on objective criteria. While the primary focus of this reevaluation is based on work with nonhuman animals, considerations are also drawn from converging evidence from cognitive psychology, neuropsychology, and cognitive neuroscience. Implications of this rethinking are discussed, as well as considerations of familiarity, indirect measures of memory, and generally what should be viewed as necessary for episodic memory. This perspective is intended to begin an iterative process within the field to redefine the meaning of episodic memory and to ultimately establish a consensus view. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
Rethinking the Definition of Episodic Memory
Christopher R. Madan
University of Nottingham
The definition of episodic memory, as proposed by Tulving, includes a requirement of conscious recall.
As we are unable to assess this aspect of memory in nonhuman animals, many researchers have referred
to demonstrations of what would otherwise be considered episodic memory as “episodic-like memory.”
Here the definition of episodic memory is reconsidered based on objective criteria. While the primary
focus of this reevaluation is based on work with nonhuman animals, considerations are also drawn from
converging evidence from cognitive psychology, neuropsychology, and cognitive neuroscience. Impli-
cations of this rethinking are discussed, as well as considerations of familiarity, indirect measures of
memory, and generally what should be viewed as necessary for episodic memory. This perspective is
intended to begin an iterative process within the field to redefine the meaning of episodic memory and
to ultimately establish a consensus view.
Public Significance Statement
Being able to remember our past experiences, such as the specific event details from a recent dinner
with friends or when you moved to a new city, rely on episodic memory. Based on the conventional
definition proposed by Endel Tulving decades ago, only humans have episodic memory and it is
inexplicably intertwined with consciousness and introspection. Here I suggest we rethink this
definition based on criteria that can be externally verified and objectively evaluated.
Keywords: episodic memory, nonhuman animals, recollection, hippocampus
Most of us can think back to the previous week (e.g., a recent
dinner with friends) and events of importance (e.g., moving to a
new place) without much difficulty. Can nonhuman animals en-
gage in similar behaviour? By the current definition of episodic
memory, this inability to peer into the introspective behaviours of
nonhuman animals means we can only ascribe evidence of
“episodic-like” memory to them. This approach seems overly
limited and anthropocentric. Here I suggest that we shift toward
more objective criteria for defining episodic memory that do not
rely on introspection or necessitate conscious recollection. The
implications of this rethinking are discussed, as well as consider-
ations of familiarity, indirect measures of memory, and generally
what should be viewed as necessary for episodic memory. Epi-
sodic memory is studied in a variety of subfields within psychol-
ogy, including cognitive psychology, neuropsychology, and cog-
nitive neuroscience, in addition to comparative psychology. In this
article, I draw from converging evidence from all of these sub-
fields to suggest a path forward that may be consistently and
broadly used. By adopting a new definition that can be externally
verified, objectively evaluated, and less reliant on self-report,
episodic memory can be more consistently assessed across a
variety of subfields. This perspective is intended to begin an
iterative process within the field to redefine the meaning of epi-
sodic memory and to ultimately establish a consensus view.
The current definition of episodic memory, as described in
(Tulving, 2002), includes a rich characterisation of the concept:
Episodic memory is a recently evolved, late-developing, and early
deteriorating past-oriented memory system, more vulnerable than
other memory systems to neuronal dysfunction, and probably unique
to humans. It makes possible mental time travel through subjective
time, from the present to the past, thus allowing one to reexperience,
through autonoetic awareness, one’s own previous experiences. Its
operations require, but go beyond, the semantic memory system.
Retrieving information from episodic memory (remembering or con-
scious recollection) is contingent on the establishment of a special
mental set, dubbed episodic “retrieval mode.” Episodic memory is
subserved by a widely distributed network of cortical and subcortical
brain regions that overlaps with but also extends beyond the networks
subserving other memory systems. The essence of episodic memory
lies in the conjunction of three concepts: self, autonoetic awareness,
and subjectively sensed time. (p. 5)
Critically, Tulving drew a direct and unambiguous correspon-
dence between systems of memory (episodic, semantic, and pro-
cedural) and the involvement of consciousness, with episodic
memory corresponding to autonoetic (self-knowing) conscious-
ness. Based on this definition, often it is suggested that animals
have “episodic-like memory,” rather than episodic memory itself,
The author thanks Daniela Palombo for insightful discussions that
helped refine the ideas presented in this article.
Correspondence concerning this article should be addressed to XChristopher
R. Madan, School of Psychology, University of Nottingham, Nottingham NG7
2RD, United Kingdom. E-mail: christopher.madan@nottingham.ac.uk
Canadian Journal of Experimental Psychology /
Revue canadienne de psychologie expérimentale
ISSN: 1196-1961 2020, Vol. 74, No. 3, 183–192
© 2020 Canadian Psychological Association http://dx.doi.org/10.1037/cep0000229
183
... This distinction between non-declarative and declarative memory is also presented as an implicit (unconscious)/explicit (conscious) memory distinction, the non-declarative memory being understood as implicit and the declarative memory as explicit. This explicit/implicit distinction does not seem to be well suited, because for example some non-declarative memory may be rehearsed with consciousness (Cabeza and Moscovitch, 2013;Ferbinteanu, 2019;Henke, 2010;Madan, 2020). Following this first non-declarative/declarative division, the systems were classified according to the behavior they result in and their neural bases: Non-declarative memory has been divided into four systems, and declarative memory into two (Camina and Güell, 2017;Squire and Zola-Morgan, 1988) ...
... Thus, animals are told to have an episodic-like memory. While being quite old, the debate is still standing, and some authors recently proposed to redefine EM without that consciousness part, allowing animals to have an EM (Madan, 2020). ...
... Eacott and Alexander Easton suggest to use a broader definition of the temporal condition, adapting the What-Where-When to a What-Where-Which (context or occasion) paradigm (Eacott and Easton, 2010;Easton and Eacott, 2008). These tasks have been widely used in animal research, allowing for the demonstration of an episodic-like memory in rodents, nonhuman primates, dolphins, dogs, horses, insects and cuttlefish (for review, see: Madan, 2020). ...
Thesis
Full-text available
Episodic memory concerns the re-experience of past personal events anchored in their encoding context. These episodic memories are not fixed: their content is influenced by the sensory modality of the recall cue. For example, memories evoked by smells are known to be less frequent, more surprising, vivid, emotional, and older than memories evoked by images or words. These phenomena are commonly explained by the close and direct anatomical links that exist between the primary olfactory, memory, and emotional brain structures. However, odors have rarely been compared to cues that also possess privileged links to memory, such as music and faces, both behaviorally and functionally. This thesis has two main objectives: 1) To identify and characterize the particularities of episodic memory attributable to the sensory modality of the recall cue (Studies 1 and 2); 2) To study the dynamics of the neural networks underlying episodic recall and more specifically the interactions that are modulated differently according to the sensory modality of the recall cue (Study 3). To test the hypothesis that emotion would be an essential factor in the particularity of olfactory cues to recall a memory, the secondary aim of this thesis is to evaluate the differential effect of emotion of the episodic recall cue as a function of its sensory modality. To meet our objectives and to allow for the study of episodic memory in the most ecological conditions possible, we have developed a non-immersive virtual reality protocol that can be declined in several versions allowing the encoding and recall of complex and multisensory episodes experienced in the laboratory. By using neutral stimuli, the first study showed that the sensory modality of the recall cue influenced recognition and episodic memory performance. Faces were very well recognized and very good cues for episodic memory; smells were less well recognized, but were good cues for episodic memory; musical excerpts, although very well recognized were not good cues for episodic memory. By using emotional stimuli, the second study confirmed the previous results, and clarified the effects of emotion on episodic memory performance by showing that the emotional valence of the recall cue favors globally all memory stages. The most pleasant and unpleasant stimuli, compared to the most neutral ones, were associated with better memory performance. In addition, the pronounced effectiveness of odors in evoking episodic recall was associated with participants’ individual motivation to resample the stimulus. This study also highlighted the importance of the ecological relevance of the stimuli, with the virtualization of faces leading to the suppression of their superiority as a memory cue in comparison to odors and music. The third study, still in progress, confirms the memory strength of odors, when they are pleasant, to recall the different dimensions of an episode. Preliminary data suggest that musical and olfactory cues in episodic memory activate autobiographical memory networks. In conclusion, our studies reveal an effect of the sensory modality of the recall cue on episodic recall and suggest that this effect is associated with the emotion carried by these cues. Odors appear to be singular recall cues, associated with average recognition performance, but favoring accurate recollection of episodic memories. This recollection is driven by the motivation the odors have generated. Music, although very well recognized, leads to less correct recall of associated episodic dimensions. Finally, visual stimuli seem to differ according to their ecological relevance, with more efficient cueing and more complete memory being associated with more ecologically relevant stimuli.
... There is evidence that fish, birds, rodents, and primates remember whatwhen-where information about events, and that great apes also remember which individual (who) performed an action (reviewed in ref. 21). These abilities have been referred to as episodic-like memory 22,23 (but see ref. 24), since it remains unknown whether non-human animals include the self in their memories. ...
... Insect consumption has been present throughout primate evolution 26 , including in modern humans 27 . Insects were important foods for early primates 26 , but their role in their cognitive evolution has only rarely been investigated 24 , mostly in the context of tool-use planning 28,29 . Chimpanzee insectivory varies in target species, dietary relevance 26 , and foraging strategies, including tool use, by site 30,31 . ...
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... Empirical work has demonstrated a potential intensity-dependent effect of acute exercise on cognition; moderate-intensity acute exercise may improve prefrontal cortex-dependent higher-order cognition (Chang, Labban, Gapin, & Etnier, 2012), such as executive control, whereas vigorous-intensity acute exercise may improve highly automated behavior (McMorris, 2016). Whether these intensity-dependent effects of acute exercise on global cognition extend to specific cognitive parameters, such as long-term episodic memory (defined as the remembrance of one's own previous experiences; Madan, 2020), is less clear (Loprinzi, Roig, Etnier, Tomporowski, & Voss, 2021e) and requires additional empirical investigation. ...
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Accumulating research demonstrates that acute exercise can enhance long-term episodic memory. However, it is unclear if there is an intensity-specific effect of acute exercise on long-term episodic memory function and whether this is influenced by the post-exercise recovery period, which was the primary objective of this experiment. Another uncertainty in the literature is whether aerobic endurance influences the interaction between exercise intensity and post-exercise recovery period on long-term episodic memory function, which was a secondary objective of this study. With exercise intensity and post-exercise recovery period occurring as within-subject factors, and fitness as a between-subject factor, 59 participants (Mage = 20 years) completed 12 primary laboratory visits. These visits included a 20-min bout of exercise (Control, Moderate, and Vigorous), followed by a recovery period (1, 5, 10, and 15 min) and then a word-list episodic memory task, involving an encoding phase and two long-term recall assessments (20-min and 24-h delayed recall). The primary finding from this experiment was that moderate and vigorous-intensity exercise improved memory function when compared to a non-exercise control. A secondary finding was that individuals with higher levels of aerobic endurance, compared to their lesser fit counterparts, had greater memory performance after exercise (moderate or vigorous) when compared to after a control condition. Additionally, individuals with higher levels of aerobic endurance, compared to their lesser fit counterparts, generally performed better on the memory task with longer post-exercise recovery periods. Future research should carefully consider these parameters when evaluating the effects of acute exercise on long-term episodic memory.
... The analysis of the data revealed five distinct themes, namely: Subsequently, some individuals activate and retrieve information from episodic memory, which has been defined as the memory of everyday events that can be consciously recalled and/or explicitly stated. These memories are very detailed and include contextual information such as time and place but also associated emotions (Madan, 2020). Yet, it appears that individuals access a more specific part of the episodic memory system-episodic self-knowledge, which entails memories of specific events involving the self, for example, personal episodes (autobiographical memories) to identify when their behaviors were congruent or incongruent with specific personality traits (Sakaki, 2007). ...
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... The biases may not be as strong, given that in Experiment 1b, where the ranges are closer together, there were more recalls outside of the prescribed ranges and more confusions between nearby ranges. More generally, the relationship between the operant-like learning involved in decisions-from-experience tasks and the role of episodic memory is not yet well understood (Madan, 2020;. Both our behavioural and modelling results shed light on this relationship and provide evidence against direct episodic recalls of events and casts doubt on models that exclusively rely on individual samples of items from memory (Bornstein et al., 2017;Gonzalez et al., 2003;Hotaling, Donkin, Jarvstad, & Newell, 2022). ...
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... Given that~6.2 million adults ≥65 years in the United States have AD 3 and the population of adults ≥65 years is projected to reach 88 million by 2050 4 , it is increasingly important to study EM. EM is the remembrance of past personal events and experiences, and it is supported by a distributed network of cortical and subcortical brain structures, including the involvement of the hippocampus and the prefrontal cortex 1,5,6 . A decline in EM is associated with a decrease in the ability to perform activities of daily living and an increase in social isolation 7,8 . ...
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