Network-centered homeostasis through inhibition maintains hippocampal spatial map and cortical circuit function

Abstract

Despite ongoing experiential change, neural activity maintains remarkable stability. Such stability is thought to be mediated by homeostatic plasticity and is deemed to be critical for normal neural function. However, what aspect of neural activity does homeostatic plasticity conserve, and how it still maintains the flexibility necessary for learning and memory, is not fully understood. Homeostatic plasticity is often studied in the context of neuron-centered control, where the deviations from the target activity for each individual neuron are suppressed. However, experimental studies suggest that there are additional, network-centered mechanisms. These may act through the inhibitory neurons, due to their dense network connectivity. Here we use a computational framework to study a potential mechanism for such homeostasis, using experimentally inspired, input-dependent inhibitory plasticity (IDIP). In a hippocampal CA1 spiking model, we show that IDIP in combination with place tuned input can explain the formation of active and silent place cells, as well as place cells remapping following optogenetic silencing of active place cells. Furthermore, we show that IDIP can also stabilise recurrent network dynamics, as well as preserve network firing rate heterogeneity and stimulus representation. Interestingly, in an associative memory task, IDIP facilitates persistent activity after memory encoding, in line with some experimental data. Hence, the establishment of global network balance with IDIP has diverse functional implications and may be able to explain experimental phenomena across different brain areas.