Spatially dispersed synapses yield sharply-tuned place cell responses through dendritic spike initiation

Abstract

The literature offers evidence for a critical role of spatially-clustered iso-feature synapses in eliciting dendritic spikes essential for sharp feature selectivity, with apparently contradictory evidence demonstrating spatial dispersion of iso-feature synapses. Here, we reconcile this apparent contradiction by demonstrating that the generation of dendritic spikes, the emergence of an excitatory ramp in somatic voltage responses and sharp tuning of place-cell responses are all attainable even when iso-feature synapses are randomly dispersed across the dendritic arbor. We found this tuning sharpness to be critically reliant on dendritic sodium and transient potassium channels and on N-methyl-D-aspartate receptors. Importantly, we demonstrate that synaptic potentiation targeted to afferents from one specific place field is sufficient to effectuate place-field selectivity even when intrinsically disparate neurons received randomly dispersed afferents from multiple place-field locations. These conclusions proffer dispersed localization of isofeature synapses as a strong candidate for achieving sharp feature selectivity in neurons across sensory-perceptual systems.\n\nO_LSTHighlightsC_LSTO_LISystematic analysis of four synaptic localization profiles for sharp spatial tuning\nC_LIO_LIDendritic spikes are generated even with randomly dispersed iso-feature synapses\nC_LIO_LISharp feature tuning could be achieved even in the absence of synaptic clusters\nC_LIO_LITargeted, yet dispersed, synaptic plasticity sufficient for place-cell emergence\nC_LI