Interaction of short-term neuronal plasticity and synaptic plasticity revealed by nonlinear systems analysis in dentate granule cells

Abstract

Dentate granule cells receive inputs from the entorhinal cortex as the "perforant path". There are two components of the perforant path: the lateral component (LPP) and the medial component (MPP). LPP and MPP convey different sensory modality information. It remains elusive as to how signals from different inputs interact and integrate at the granule cell level. We attempted to address this issue by using nonlinear systems analytic methods. Granule cell EPSPs and action potentials were recorded intracellularly from in vitro hippocampal slices of the rat. MPP and LPP were activated simultaneously by two independent Poisson random trains. Poisson-Volterra kernel models were estimated using Laguerre expansion of Volterra kernel technique. In the kernel models, self-kernels represent the intrinsic input/output properties of each pathway, while cross-kernels quantify the interactions between the two inputs. Short-term plasticity (STP) was revealed by both 2nd order self and cross kernels. We reason that the underlying mechanisms of the STP are diffusely distributed along input-specific synapses, dendritic tree and soma. The plasticity held by the dendritic tree/soma and synapses can be divided and referred to as neuronal and synaptic plasticity respectively. We argue that the cross kernel properties are determined primarily by neuronal plasticity while the self kernel properties are controlled largely by synaptic plasticity. Our experimental data suggest that linear summation of the membrane potential of the postsynaptic neuron can only partially explain the neuronal plasticity. Both supra- and sublinear summations were observed. Thus, the neuronal plasticity is likely to be the product of passive and active processes of the postsynaptic neuron and plays a pivotal role in multiple inputs integration.