Recent years have seen a resurgence in use of the extracellularly recorded local field potential (LFP) to investigate neural network activity. To probe monosynaptic thalamic activation of cortical postsynaptic target cells, so called spike-trigger-averaged LFP (stLFP) signatures have been measured. In these experiments the cortical LFP is measured by means of multielectrodes covering several cortical lamina and averaged on spontaneous spikes of thalamocortical (TC) cells. Using a well-established forward-modeling scheme, we investigate the biophysical origin of this stLFP signature with simultaneous synaptic activation of cortical layer 4 neurons, mimicking the effect of a single afferent spike from a single TC neuron. Constrained by previously measured intracellular responses of the main postsynaptic target cell types and with biologically plausible assumptions regarding the spatial distribution of thalamic synaptic inputs into layer 4, the model predicted characteristic contributions to monosynaptic stLFP signatures both for the regular spiking (RS) excitatory neurons and the fast spiking (FS) inhibitory interneurons. In particular, the FS cells generated stLFP signatures of shorter temporal duration than the RS cells. Added together, a sum of the stLFP signatures of these two principal synaptic targets of thalamocortical cells were observed to resemble experimentally measured stLFP signatures. Outside the volume targeted by TC afferents the resulting postsynaptic LFP signals were found to be sharply attenuated. This implies that such stLFP signatures provide a very local measure of thalamocortical synaptic activation, and that newly developed inverse CSD-estimation methods are needed for precise assessment of the underlying spatiotemporal current-source density (CSD) profiles.
Despite its long history and prevalent use, the proper interpretation of the extracellularly recorded local field potential (LFP) is still not fully established. Here we investigate by means of biophysical modeling the origin of the focal LFP signature of the single-axon monosynaptic thalamocortical connection as measured by spike-trigger-averaging of cortical LFPs on spontaneous spikes of thalamocortical neurons. We find that this LFP signature is well accounted for by a model assuming thalamic projections to two cortical layer-4 cell populations: one excitatory (putatively regular-spiking cells) and one inhibitory (putatively fast-spiking cells). The LFP signature is observed to decay sharply outside the cortical region receiving the thalamocortical projection, implying that it indeed provides a very local measure of thalamocortical synaptic activation.
The authors declare no conflict of interest
This work was supported by the Research Council of Norway (NOTUR, NevroNor, CoBra), the Helmholtz Portfolio Supercomputing and Modeling for the Human Brain (SMHB), the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement n° 604102 (HBP) and the National Institutes of Health (NIH) through NIH grants EYO5253 and MHO85357.
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