Evidence for remembering when events occurred in a rodent model of episodic memory

Department of Psychology, University of Georgia, Athens, GA 30602-3013, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 06/2009; 106(23):9525-9. DOI: 10.1073/pnas.0904360106
Source: PubMed


The content of episodic memory consists of representations of unique past events. Episodic memories are grounded in a temporal framework (i.e., we remember when an event occurred). It has recently been argued that episodic-like memory in rats is qualitatively different from human episodic memory because, rather than remembering when an earlier past event occurred, rats used the cue of how long ago it occurred. We asked, therefore, whether rats remember the time of day at which they encountered a distinctive event, in addition to what occurred and where it happened. Rats were tested in the morning and afternoon, on separate days. A distinctive flavor (chocolate) was replenished at a daily-unique location at only one of these times. The interval between first and second daily opportunities to eat (study and test, respectively) was constant. Rats adjusted their revisits to the chocolate location at different times of day by using time of day rather than the cue of how long ago an event occurred. Two lines of evidence suggest that rats remembered the time at which the distinctive event occurred. First, under conditions in which the time of test (but not time of study) was novel, rats immediately transferred their knowledge of the chocolate contingency to the new test time. Second, under conditions in which predictions for study and test times were put in conflict, rats again used study time. Our results suggest that, at the time of memory assessment, rats remember when a recent episode occurred, similar to human episodic memory.

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    • "The criterion for episodic-like memory is that a behavioral response should be based on "what" occurred "where" and "when" during a past experience (Clayton and Dickinson 1998; see also above). What–where–when memory as a form of episodic-like memory was first proposed in an elegant study on Western scrub jays (Clayton and Dickinson 1998) and later in rats (Zhou and Crystal 2009). Although the computational, cellular and neuroanatomical processes underlying spatial memory are often assumed also to control episodic memory (Buzsáki and Moser 2013), none of the traditional tests used in mice and rats assess episodic-like memory (Morris 2001). "
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    ABSTRACT: The analysis of spatial learning and memory in rodents is commonly used to investigate the mechanisms underlying certain forms of human cognition and to model their dysfunction in neuropsychiatric and neurodegenerative diseases. Proper interpretation of rodent behavior in terms of spatial memory and as a model of human cognitive functions is only possible if various navigation strategies and factors controlling the performance of the animal in a spatial task are taken into consideration. The aim of this review is to describe the experimental approaches that are being used for the study of spatial memory in rats and mice and the way that they can be interpreted in terms of general memory functions. After an introduction to the classification of memory into various categories and respective underlying neuroanatomical substrates, I explain the concept of spatial memory and its measurement in rats and mice by analysis of their navigation strategies. Subsequently, I describe the most common paradigms for spatial memory assessment with specific focus on methodological issues relevant for the correct interpretation of the results in terms of cognitive function. Finally, I present recent advances in the use of spatial memory tasks to investigate episodic-like memory in mice.
    Cell and Tissue Research 06/2013; 354(1). DOI:10.1007/s00441-013-1668-9 · 3.57 Impact Factor
    • "Remarkably there is a clear lack of agreement in the way that the temporal component has been operationalized. In some studies when is considered as “in which occasion” [e.g., order of events (Eichenbaum et al., 2005; Eacott and Easton, 2010)], in others defined when is defined as sensitivity to “how long ago” the caching/baiting event took place (Clayton and Dickinson, 1998; Clayton et al., 2003b) and in others “when” is defined as “in which moment” (Roberts et al., 2008; Zhou and Crystal, 2009). In fact, the extent to what remembering “order of events” require the same memory system as remembering “how long ago” is still an open question (Easton et al., 2012). "
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    ABSTRACT: Historically, episodic memory has been described as autonoetic, personally relevant, complex, context-rich, and allowing mental time travel. In contrast, semantic memory, which is theorized to be free of context and personal relevance, is noetic and consists of general knowledge of facts about the world. The field of comparative psychology has adopted this distinction in order to study episodic memory in non-human animals. Our aim in this article is not only to reflect on the concept of episodic memory and the experimental approaches used in comparative psychology to study this phenomenon, but also to provide a critical analysis of these paradigms. We conclude the article by providing new avenues for future research.
    Frontiers in Behavioral Neuroscience 06/2013; 7(63):63. DOI:10.3389/fnbeh.2013.00063 · 3.27 Impact Factor
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    • "Degradation of the capacity to store and retrieve episodic memories results from several neuropsychiatric diseases , with dramatic consequences for the affected patients and their families. The original definition of episodic memory has been linked to autonoetic consciousness (Tulving, 2002), a feature that can be demonstrated only in humans (Griffiths et al., 1999). For nonhuman animals, the definition of episodic-like memory has been proposed. "
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    ABSTRACT: Episodic memory is relevant for auto-consciousness in humans. In nonhuman animals, episodic-like memory is defined when the "what-where-when" content of a unique event forms an integrated cognitive representation that is then deployed during memory retrieval. Here, we aimed at testing episodic-like memories of mice under experimental conditions that allow the analysis of whether and how mice process what-where-when information. Using an ecologically relevant paradigm for spontaneous learning and memory, we show that mice modulate their behavior based on the what, where, and when components of past unique episodes, specifically on previous encounters of conspecifics at a defined location and at a specific time of the day. We also show that learning during this paradigm activated Arc/Arg3.1 mRNA expression in the hippocampus and that stereotactic injection of anisomycin into this region impairs memory consolidation. Thus, hippocampus-dependent episodic-like memories of single experiences are spontaneously created in mice. These findings extend our knowledge of the cognitive capacities of the mouse and suggest that this species can be used as model for studying the mechanisms underlying human episodic memory and related neurological disorders.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 01/2013; 33(3):1038-43. DOI:10.1523/JNEUROSCI.2280-12.2013 · 6.34 Impact Factor
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