Long-term potentiation expands information content of hippocampal dentate gyrus synapses

Significance Understanding plasticity processes in the hippocampus is critical to our understanding of the biological underpinnings of memory. By applying information theory to quantify information content at synapses, we demonstrate that induction of long-term potentiation (LTP) increases the storage capacity of synapses in hippocampal dentate gyrus. Nevertheless, even after LTP, the information storage capacity of dentate synapses was much lower than in a different part of the hippocampus, area CA1. This work lays a foundation for future studies elucidating the time course for increased information storage content as well as the basis for interregion variability in information storage capacity. An approach combining signal detection theory and precise 3D reconstructions from serial section electron microscopy (3DEM) was used to investigate synaptic plasticity and information storage capacity at medial perforant path synapses in adult hippocampal dentate gyrus in vivo. Induction of long-term potentiation (LTP) markedly increased the frequencies of both small and large spines measured 30 minutes later. This bidirectional expansion resulted in heterosynaptic counterbalancing of total synaptic area per unit length of granule cell dendrite. Control hemispheres exhibited 6.5 distinct spine sizes for 2.7 bits of storage capacity while LTP resulted in 12.9 distinct spine sizes (3.7 bits). In contrast, control hippocampal CA1 synapses exhibited 4.7 bits with much greater synaptic precision than either control or potentiated dentate gyrus synapses. Thus, synaptic plasticity altered total capacity, yet hippocampal subregions differed dramatically in their synaptic information storage capacity, reflecting their diverse functions and activation histories.