Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments

By Loren M. Frank, G. B. Stanley, Emery N. Brown. 2004

383 citations recorded by the source corpus.

The hippocampus is essential for learning complex spatial relationships, but little is known about how hippocampal neural activity changes as animals learn about a novel environment. We studied the formation of new place representations in rats by examining the changes in place-specific firing of neurons in the CA1 region of the hippocampus and the relationship between these changes and behavioral change across multiple days of exposure to novel places. We found that many neurons showed very rapid changes on the first day of exposure to the novel place, including many cases in which a previously silent neuron developed a place field over the course of a single pass through the environment. Across the population, the largest changes in neural activity occurred on day 2 of exposure to a novel place, but only if the animal had little experience (<4 min) in that location on day 1. Longer exposures on day 1 were associated with smaller changes on day 2, suggesting that hippocampal neurons required 5-6 min of experience to form a stable spatial representation. Even after the representation stabilized, the animals' behavior remained different in the novel places, suggesting that other brain regions continued to distinguish novel from familiar locations. These results show that the hippocampus can form new spatial representations quickly but that stable hippocampal representations are not sufficient for a place to be treated as familiar.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neurology

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Citations in the corpus

Awake replay of remote experiences in the hippocampus (2009, positive): “After the animals alternated reliably for liquid reward (sweetened condensed milk), they were implanted with a microdrive array containing 30 independently movable tetrodes targeting CA3 and CA120, 27 according to UCSF and NIH guidelines.”
Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory (2005, background): “In contrast, place cells may become omnidirectional minutes after the animal is introduced into a 2-dimensional environment and they remain omnidirectional (O’Keefe and Nadel, 1978; Muller and Kubie, 1987; Wilson and McNaughton, 1993; Muller et al., 1994; Markus et al., 1995; Frank et al., 2005).”
New experiences enhance coordinated neural activity in the hippocampus. (2008, positive): “Overall, our results for phase precession and the sequence compression index are compatible with the 2–3 day time course of place field formation seen in our previous work (Frank et al., 2004).”
Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. (2008, background): “As reported previously for the dorsal hippocampus (Frank et al., 2004; Leutgeb et al., 2004; Wilson and McNaughton, 1993), place fields in CA1 were broader and more irregular in a novel environment than in an environment where the animal had been trained for several weeks.”
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus (2009, positive): “6 mm AP; 3.4mm L) using previously described methods (Frank et al., 2004).”
Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration (2007, background): “However, we observed firing rate changes during exploration in novel environments relative to familiar ones, as previous studies have shown (Wilson & McNaughton, 1993; Hirase et al., 2001; Frank et al., 2004; Nitz & McNaughton, 2004).”
Network dynamics underlying the formation of sparse, informative representations in the hippocampus (2008, positive): “Furthermore, whereas CA1 cells undergo rapid plasticity in novel environments (Wilson and McNaughton, 1993), CA1 place field plasticity (Austin et al., 1993; Frank et al., 2004) and novelty-specific reactivation (Cheng and Frank, 2008) can extend beyond the first day of exposure to a new place.”
Place cells, grid cells, and the brain's spatial representation system. (2008, background): “When animals explore new environments, it takes several minutes for the firing fields to reach a stable state (Hill 1978, Wilson & McNaughton 1993, Frank et al. 2004).”
Dissociating the past from the present in the activity of place cells (2006, background): “In fact, when placed in a novel environment, cells can develop stable location-selective firing after a single pass over the field location (Frank et al., 2004), although this is not true of all cells.”
Entorhinal Cortical Ocean Cells Encode Specific Contexts and Drive Context-Specific Fear Memory. (2015, positive): “These values are not significantly different from the latencies of CA1 place cells of about 50 s (Frank et al., 2004) and entorhinal grid cells of 60 s (Hafting et al.”