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      Watching a memory form—VSD imaging reveals a novel memory mechanism

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          ABSTRACT

          Studies of the mechanisms underlying memory formation have largely focused on the synapse. However, recent evidence suggests that additional, non-synaptic, mechanisms also play important roles in this process. We recently described a novel memory mechanism whereby a particular class of neurons was recruited into the Tritonia escape swim network with sensitization, a non-associative form of learning. Neurons that in the naïve state were loosely-affiliated with the network were rapidly recruited in, transitioning from variably bursting (VB) to reliably bursting (RB). Even after the memory had faded some new neurons remained, and some original members had left, leaving the network in an altered state. Further, we identified a candidate cellular mechanism underlying these network changes. Our study supports the view that brain networks may have surprisingly fluid functional structures and adds to the growing body of evidence that non-synaptic mechanisms often operate synergistically with changes at the synapse to mediate memory formation.

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          Most cited references14

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          Long-term dynamics of CA1 hippocampal place codes

          Via Ca2+-imaging in freely behaving mice that repeatedly explored a familiar environment, we tracked thousands of CA1 pyramidal cells' place fields over weeks. Place coding was dynamic, for each day the ensemble representation of this environment involved a unique subset of cells. Yet, cells within the ∼15–25% overlap between any two of these subsets retained the same place fields, which sufficed to preserve an accurate spatial representation across weeks.
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            Neuronal competition and selection during memory formation.

            Competition between neurons is necessary for refining neural circuits during development and may be important for selecting the neurons that participate in encoding memories in the adult brain. To examine neuronal competition during memory formation, we conducted experiments with mice in which we manipulated the function of CREB (adenosine 3',5'-monophosphate response element-binding protein) in subsets of neurons. Changes in CREB function influenced the probability that individual lateral amygdala neurons were recruited into a fear memory trace. Our results suggest a competitive model underlying memory formation, in which eligible neurons are selected to participate in amemorytrace as a function of their relative CREB activity at the time of learning.
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              Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training.

              Memories are thought to be sparsely encoded in neuronal networks, but little is known about why a given neuron is recruited or allocated to a particular memory trace. Previous research shows that in the lateral amygdala (LA), neurons with increased CREB are selectively recruited to a fear memory trace. CREB is a ubiquitous transcription factor implicated in many cellular processes. Which process mediates neuronal memory allocation? One hypothesis is that CREB increases neuronal excitability to bias neuronal recruitment, although this has not been shown experimentally. Here we use several methods to increase neuronal excitability and show this both biases recruitment into the memory trace and enhances memory formation. Moreover, artificial activation of these neurons alone is a sufficient retrieval cue for fear memory expression, showing that these neurons are critical components of the memory trace. These results indicate that neuronal memory allocation is based on relative neuronal excitability immediately before training.
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                Author and article information

                Journal
                Commun Integr Biol
                Commun Integr Biol
                KCIB
                kcib20
                Communicative & Integrative Biology
                Taylor & Francis
                1942-0889
                2016
                15 August 2016
                15 August 2016
                : 9
                : 5
                : e1212142
                Affiliations
                [a ]Department of Cell Biology and Anatomy, Rosalind Franklin University , North Chicago, IL, USA
                [b ]Department of Neuroscience, Rosalind Franklin University , North Chicago, IL, USA
                Author notes
                CONTACT Evan S Hill evan.hill@ 123456rosalindfranklin.edu Department of Cell Biology and Anatomy, Rosalind Franklin University of Science and Medicine , 3333 Green Bay Rd, North Chicago, IL 60064, USA
                Article
                1212142
                10.1080/19420889.2016.1212142
                5154357
                9b577950-7099-49f8-9109-4d10286998c8
                © 2016 The Author(s). Published with license by Taylor & Francis

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-Non-Commercial License http://creativecommons.org/licenses/by-nc/3.0/, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The moral rights of the named author(s) have been asserted.

                History
                : 5 July 2016
                : 6 July 2016
                Page count
                Figures: 0, Tables: 0, References: 17, Pages: 3
                Categories
                Article Addendum

                Molecular biology
                invertebrate,learning,neuronal allocation,neuronal network,synaptic plasticity,voltage-sensitive dye

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