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Challenging the brain with experiential richness creates tissue-level changes and synaptic plasticity, but the interjacent network level has not been accessible. We here show that environmental enrichment has unexpectedly far-reaching effects on network connectivity and multi-dimensional coding in the hippocampus. We present direct evidence that experience impacts local and global network connectivity, synchrony, and rhythmic dynamics. For this, we investigated the hippocampi from standard-housed mice (SD) and mice living in an enriched environment (ENR) using large-scale ex vivo recordings with a high-density microelectrode sensing array that with the unprecedented spatiotemporal resolution allowed simultaneous electrophysiological assessment across the entire circuit. In the absence of extrinsic electrical network stimulation, we found enhanced functional connectivity and high-dimensional coding in hippocampal-cortical networks of ENR mice. The mapped connectome illustrated a scale-free small-world topology and an ENR-induced resilience to random failures. ENR enhanced large-scale spatiotemporal firing patterns, which facilitated efficient pattern separation and boosted the information encoded in the firing phases of slow oscillatory rhythms. Given that essentially all electrophysiological studies on network behaviors have been done on animals housed in stimulus-poor conditions, our SD mice showed the expected normal functionality. The literature consequently underestimates the extent of spontaneous network activity and connectivity under truly physiological conditions. Our results pave the way to unveil fundamental mechanisms of experience-dependent enhancement in the hippocampal network underlying high brain functions and provide markers for large-scale network remodeling and metaplasticity.

Large-scale multi-site biosensors are essential to probe the olfactory bulb (OB) circuitry for understanding the spatiotemporal dynamics of simultaneous discharge patterns. Current ex-vivo electrophysiological techniques are limited to recording a small set of neurons and cannot provide an inadequate resolution, which hinders revealing the fast dynamic underlying the information coding mechanisms in the OB circuit. Here, we demonstrate a novel biohybrid OB-CMOS platform to decipher the cross-scale dynamics of OB electrogenesis and quantify the distinct neuronal coding properties. The approach with 4096-microelectrodes offers a non-invasive, label-free, bioelectrical imaging to decode simultaneous firing patterns from thousands of connected neuronal ensembles in acute OB slices. The platform can measure spontaneous and drug-induced extracellular field potential activity. We employ our OB-CMOS recordings to perform multidimensional analysis to instantiate specific neurophysiological metrics underlying the olfactory spatiotemporal coding that emerged from the OB interconnected layers. Our results delineate the computational implications of large-scale activity patterns in functional olfactory processing. The high-content characterization of the olfactory circuit could benefit better functional interrogations of the olfactory spatiotemporal coding, connectivity mapping, and, further, the designing of reliable and advanced olfactory cell-based biosensors for diagnostic biomarkers and drug discovery.