Differences in Hippocampal Neuronal Population Responses to Modifications of an Environmental Context: Evidence for Distinct, Yet Complementary, Functions of CA3 and CA1 Ensembles

By A. Vazdarjanova, John Guzowski. 2004

503 citations recorded by the source corpus.

Understanding how the hippocampus processes information critical for establishing spatial and declarative memories will benefit greatly from determining not only what kind of information the hippocampus registers, but also how this information is processed across the different hippocampal subfields. We addressed this question using a novel immediate-early gene-based brain-imaging method (Arc/H1a catFISH) that allows comparisons of neuronal ensembles activated by two experiences separated by ∼30 min. Rats exposed to the same environment twice activated CA3 and CA1 ensembles with a similarly high degree of overlap. Changing the identity or configuration of local cues, or changing distal cues, activated CA3 and CA1 ensembles with reduced overlap. Yet, the overlap was greater in CA3 than in CA1. In contrast, rats exposed to two completely different environments activated CA3 and CA1 ensembles with low overlap, and this overlap was even lower in CA3 compared with CA1. Thus, CA3 has a discontinuous, whereas CA1 has a graded, population response to alterations of an environment. Additionally, as indicated by the percentage of active neurons, the context representation was more sparse in CA3 (∼18%) than in CA1 (∼35%). Finally, CA3 and CA1 activity levels were not correlated within a session, arguing against a simple coactivation of these regions. Instead, the within-rat ratio of CA3/CA1 cell activity was correlated across sessions, suggesting that the balance of CA3/CA1 activity is individual specific. Taken together, these findings suggest that CA3 and CA1 neuronal ensembles perform distinct, yet complementary, functions in the processing of spatial and contextual information.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neurology

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Citations in the corpus

Place cells, grid cells, and the brain's spatial representation system. (2008, background): “The disambiguation of the firing patterns is stronger in CA3 than in CA1 (Leutgeb et al. 2004, Vazdarjanova & Guzowski 2004).”
Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. (2008, background): “This influence may mediate the output of pattern completion mechanisms in the associative network of CA3 (Lee et al., 2004; Nakazawa et al., 2002; Vazdarjanova and Guzowski, 2004), which could have a role in generating spatial representations of familiar environments in CA1 independently of the…”
Tracking the Flow of Hippocampal Computation: Pattern Separation, Pattern Completion, and Attractor Dynamics (2015, background): “…from other laboratories have shown evidence that the CA3 representations are completely independent under more extreme conditions that would presumably generate a larger Δinput from EC, (Leutgeb, Leutgeb, Treves, Moser, & Moser, 2004; Vazdarjanova & Guzowski, 2004; Guzowski et al., 2004).”
Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas (2006, methodology): “Novelty exploration is one procedure which has been shown by Guzowski and colleagues to cause an up-regulation of the immediate early gene Arc (Guzowski et al., 1999; Vazdarjanova & Guzowski, 2004).”