Shared Neural Ensemble links Distinct Contextual Memories

Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Nature 534, 115–118 (02 June 2016)

A shared neural ensemble links distinct contextual memories encoded close in time

Departments of Neurobiology, Psychiatry & Biobehavioral Sciences and Psychology, Integrative Center for Learning and Memory, Brain Research Institute, University of California, Los Angeles, California 90095, USA

Departments of Neurology and Psychiatry & Biobehavioral Sciences, Integrative Center for Learning and Memory, Brain Research Institute, University of California, Los Angeles, California 90095, USA

West Los Angeles VA Medical Center, 11301 Wilshire Blvd, Los Angeles, California 90073, USA

Department of Neurosciences, University of California, San Diego, La Jolla, California 92093, USA

Veterans Affairs Medical Center, San Diego, California 92161, USA

Departments of Cell Biology and Neurosciences, Institute for Childhood and Neglected Diseases, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037, USA

Division of Hematology/Oncology, David Geffen School of Medicine, University of California, Los Angeles, California 90095, USA

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Recent studies suggest that a shared neural ensemble may link distinct memories encoded close in time. According to the memory allocation hypothesis, learning triggers a temporary increase in neuronal excitability that biases the representation of a subsequent memory to the neuronal ensemble encoding the first memory, such that recall of one memory increases the likelihood of recalling the other memory. Here we show in mice that the overlap between the hippocampal CA1 ensembles activated by two distinct contexts acquired within a day is higher than when they are separated by a week. Several findings indicate that this overlap of neuronal ensembles links two contextual memories. First, fear paired with one context is transferred to a neutral context when the two contexts are acquired within a day but not across a week. Second, the first memory strengthens the second memory within a day but not across a week. Older mice, known to have lower CA1 excitability, do not show the overlap between ensembles, the transfer of fear between contexts, or the strengthening of the second memory. Finally, in aged mice, increasing cellular excitability and activating a common ensemble of CA1 neurons during two distinct context exposures rescued the deficit in linking memories. Taken together, these findings demonstrate that contextual memories encoded close in time are linked by directing storage into overlapping ensembles. Alteration of these processes by ageing could affect the temporal structure of memories, thus impairing efficient recall of related information.

Contextual memories are encoded in discrete and sparse populations of neurons in the hippocampus. Recent findings demonstrated that increasing the relative neuronal excitability of a subset of neurons increases the probability that those neurons will participate in a memory trace. While previous studies used viral vectors to manipulate excitability, temporary increases in excitability occur naturally following learning, including in the hippocampus. Therefore, two distinct memories could be linked across time because the temporary increase in excitability would bias the storage of a subsequent memory to many of the same neurons that encoded the first memory, such that recall of one of these events would also probably lead to recall of the other, a key prediction of the memory allocation hypothesis.

Mechanisms that link memories are critically important for organizing the enormous number of related memories stored throughout a lifetime. Our results support the memory allocation hypothesis and are consistent with human data and computational modelling, suggesting that memories encoded within close temporal proximity are more likely to be co-recalled than memories encoded across more distant time frames. Our data indicate that overlapping populations of CA1 neurons serve to link and strengthen memories, thus facilitating integrated recall of experiences encoded close in time while separating those encoded further in time. Temporary increases in excitability probably represent one of a family of mechanisms (synaptic tagging and capture is another example) that structure the acquisition and storage of information to facilitate future use and recall. Alteration of these processes, such as decreases in neuronal excitability during ageing, could affect the organization of memory thus impairing efficient recall of related information.

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