Modelling unitary fields and the single-neuron contribution to local field potentials in the hippocampus.

KEY POINTS

We simulate the unitary local field potential (uLFP) generated in the hippocampus CA3, using morphologically detailed models. The model suggests that cancelling effects between apical and basal dendritic synapses explain the low amplitude of excitatory uLFPs. Inhibitory synapses around the soma do not cancel and could explain the high-amplitude inhibitory uLFPs. These results suggest that somatic inhibition constitutes a strong component of LFPs, which may explain a number of experimental observations.

ABSTRACT

Synaptic currents represent a major contribution to the local field potential (LFP) in brain tissue, but the respective contribution of excitatory and inhibitory synapses is not known. Here, we provide estimates of this contribution by using computational models of hippocampal pyramidal neurons, constrained by in vitro recordings. We focus on the unitary LFP (uLFP) generated by single neurons in the CA3 region of the hippocampus. We first reproduce experimental results for hippocampal basket cells, and in particular how inhibitory uLFP are distributed within hippocampal layers. Next, we calculate the uLFP generated by pyramidal neurons, using morphologically reconstructed CA3 pyramidal cells. The model shows that the excitatory uLFP is of small amplitude, smaller than inhibitory uLFPs. Indeed, when the two are simulated together, inhibitory uLFPs mask excitatory uLFPs, which might create the illusion that the inhibitory field is generated by pyramidal cells. These results provide an explanation for the observation that excitatory and inhibitory uLFPs are of the same polarity, in vivo and in vitro. These results suggest that somatic inhibitory currents are large contributors to the LFP, which is important information for interpreting this signal. Finally, the results of our model might form the basis of a simple method to compute the LFP, which could be applied to point neurons for each cell type, thus providing a simple biologically grounded method for calculating LFPs from neural networks. In conclusion, computational models constrained by in vitro recordings suggest that: (1) Excitatory uLFPs are of smaller amplitude than inhibitory uLFPs. (2) Inhibitory uLFPs form the major contribution to LFPs. (3) uLFPs can be used as a simple model to generate LFPs from spiking networks.