In neural integrators, transient inputs are accumulated into persistent firing rates that are a neural correlate of short-term memory. Integrators often contain two opposing cell populations that increase and decrease sustained firing as a stored parameter value rises. A leading hypothesis for the mechanism of persistence is positive feedback through mutual inhibition between these opposing populations. We tested predictions of this hypothesis in the goldfish oculomotor velocity-to-position integrator by measuring the eye position and firing rates of one population, while pharmacologically silencing the opposing one. In complementary experiments, we measured responses in a partially silenced single population. Contrary to predictions, induced drifts in neural firing were limited to half of the oculomotor range. We built network models with synaptic-input thresholds to demonstrate a new hypothesis suggested by these data: mutual inhibition between the populations does not provide positive feedback in support of integration, but rather coordinates persistent activity intrinsic to each population.
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*NOTE: In the version of this article initially published, the labels for the x-axes in figure 8, panels c and d are incorrect. The correct labels should be “Rate, left”. This error has been corrected in the HTML and PDF versions of the article.
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We thank H.S. Seung, C. Brody and J. Raymond for helpful discussions and critique. The experimental phase of this work was supported by Bell Laboratories. E.A. holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. M.S.G. holds a Brachmann–Hoffman Fellowship from Wellesley College. All authors received support from the US National Institutes of Health.
The authors declare no competing financial interests.
Model tuning curves defined by experimentally measured rate versus position relationships. (PDF 200 kb)
Method for functional dissection of a circuit. (PDF 1071 kb)
Change in position drift for each complete left inactivation. (PDF 123 kb)
Change in rate drift for each complete left inactivation. (PDF 92 kb)
Change in rate drift for each caudal right inactivation. (PDF 89 kb)
Values of η for the model simulations. (PDF 119 kb)
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