The dentate gyrus controls hippocampal representational drift
Douglas GoodSmithiD, Antoine Madar, William H Carson, Mark E. J. SheffieldiD
Abstract
Neural representations evolve across time and experience, a phenomenon termed representational drift. The function and circuit mechanisms of drift remain unknown, including whether it reflects intrinsic biological variability within the population or is actively controlled by circuit inputs. Progress has been limited because there is currently no known experimental means to manipulate drift without also altering an animal's sensory or behavioral experience. Here we show that drift can be experimentally controlled through targeted manipulation of upstream circuit inputs. We demonstrate this principle in the hippocampus by selectively manipulating dentate gyrus granule cells, which are thought to promote discrimination between similar experiences. Inhibiting granule cells during repeated experiences in familiar virtual environments markedly reduced drift in downstream CA1, revealing that representational drift is not simply an intrinsic property of neural populations, but is actively controlled by upstream circuitry. By experimentally manipulating this circuit-level control of drift, we further discovered that hippocampal drift is concentrated around episode transitions rather than accumulating continuously throughout an experience. These findings establish experimental control over hippocampal drift, revealing a structured, circuit-regulated process that differentiates repeated experiences into distinct episodic representations.
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