Preexisting hippocampal network dynamics constrain optogenetically induced place fields

Abstract

Neuronal circuits face a fundamental tension between maintaining existing structure and changing to accommodate new information. Memory models often emphasize the need to encode novel patterns of neural activity imposed by \"bottom-up\" sensory drive. In such models, learning is achieved through synaptic alterations, a process which potentially interferes with previously stored knowledge 1-3. Alternatively, neuronal circuits generate and maintain a preconfigured stable dynamic, sometimes referred to as an attractor, manifold, or schema 4-7, with a large reservoir of patterns available for matching with novel experiences 8-13. Here, we show that incorporation of arbitrary signals is constrained by pre-existing circuit dynamics. We optogenetically stimulated small groups of hippocampal neurons as mice traversed a chosen segment of a linear track, mimicking the emergence of place fields 1,14,15, while simultaneously recording the activity of stimulated and non-stimulated neighboring cells. Stimulation of principal neurons in CA1, but less so CA3 or the dentate gyrus, induced persistent place field remapping. Novel place fields emerged in both stimulated and non-stimulated neurons, which could be predicted from sporadic firing in the new place field location and the temporal relationship to peer neurons prior to the optogenetic perturbation. Circuit modification was reflected by altered spike transmission between connected pyramidal cell - inhibitory interneuron pairs, which persisted during post-experience sleep. We hypothesize that optogenetic perturbation unmasked sub-threshold, pre-existing place fields16,17. Plasticity in recurrent/lateral inhibition may drive learning through rapid exploration of existing states.