PT - JOURNAL ARTICLE AU - Aaron D. Milstein AU - Yiding Li AU - Katie C. Bittner AU - Christine Grienberger AU - Ivan Soltesz AU - Jeffrey C. Magee AU - Sandro Romani TI - Bidirectional synaptic plasticity rapidly modifies hippocampal representations independent of correlated activity AID - 10.1101/2020.02.04.934182 DP - 2020 Jan 01 TA - bioRxiv PG - 2020.02.04.934182 4099 - http://biorxiv.org/content/early/2020/02/05/2020.02.04.934182.short 4100 - http://biorxiv.org/content/early/2020/02/05/2020.02.04.934182.full AB - According to standard models of synaptic plasticity, correlated activity between connected neurons drives changes in synaptic strengths to store associative memories. Here we tested this hypothesis in vivo by manipulating the activity of hippocampal place cells and measuring the resulting changes in spatial selectivity. We found that the spatial tuning of place cells was rapidly reshaped via bidirectional synaptic plasticity. To account for the magnitude and direction of plasticity, we evaluated two models – a standard model that depended on synchronous pre- and post-synaptic activity, and an alternative model that depended instead on whether active synaptic inputs had previously been potentiated. While both models accounted equally well for the data, they predicted opposite outcomes of a perturbation experiment, which ruled out the standard correlation-dependent model. Finally, network modeling suggested that this form of bidirectional synaptic plasticity enables population activity, rather than pairwise neuronal correlations, to drive plasticity in response to changes in the environment.