Dipolar extracellular potentials generated by axonal projections

McColgan, Thomas; Liu, Ji; Kuokkanen, Paula T.; Carr, Catherine E.; Wagner, Hermann; Kempter, Richard

doi:10.1101/109918

Cited by 3 publications

(4 citation statements)

References 64 publications

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“…Acoustic stimuli were digitally generated by a custom-made Matlab (MathWorks, Natick, MA, USA; RRID: SCR_001622 ) script ( McColgan and Liu, 2017 ) driving a signal-processing board (RX6, Tucker-Davis Technologies, Alachua, FL, USA) at a sampling rate of 195.3125 kHz. The sound stimuli were attenuated using a programmable attenuator (PA5, Tucker-Davis Technologies).…”

Section: Methodsmentioning

confidence: 99%

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Dipolar extracellular potentials generated by axonal projections

McColgan

Liu

Kuokkanen

et al. 2017

eLife

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Extracellular field potentials (EFPs) are an important source of information in neuroscience, but their physiological basis is in many cases still a matter of debate. Axonal sources are typically discounted in modeling and data analysis because their contributions are assumed to be negligible. Here, we established experimentally and theoretically that contributions of axons to EFPs can be significant. Modeling action potentials propagating along axons, we showed that EFPs were prominent in the presence of terminal zones where axons branch and terminate in close succession, as found in many brain regions. Our models predicted a dipolar far field and a polarity reversal at the center of the terminal zone. We confirmed these predictions using EFPs from the barn owl auditory brainstem where we recorded in nucleus laminaris using a multielectrode array. These results demonstrate that axonal terminal zones can produce EFPs with considerable amplitude and spatial reach.

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Section: Methodsmentioning

confidence: 99%

“…The code for these simulations is available at https://github.com/phreeza/pyLaminaris ( McColgan and Liu, 2017 ). A copy is archived at https://github.com/elifesciences-publications/pyLaminaris .…”

Section: Methodsmentioning

confidence: 99%

Dipolar extracellular potentials generated by axonal projections

McColgan

Liu

Kuokkanen

et al. 2017

eLife

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“…In Figure 6D , we model individual unmyelinated axons while varying the number of branches. Axonal branching substantially increased the surface EAP amplitude (McColgan et al 2017): a single axon with a fixed diameter of 0.3 μm and four bifurcations within the top 50 μm produced an EAP threefold higher compared to an unbranched axon.…”

Section: Resultsmentioning

confidence: 99%

Imaging through Windansee electrode arrays reveals a small fraction of local neurons following surface MUA

Thunemann

Hossain

Ness

et al. 2022

Preprint

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Prior studies have shown that neuronal spikes can be recorded with microelectrode arrays placed on the cortical surface. However, the etiology of these spikes remains unclear. Because the top cortical layer (layer 1) contains very few neuronal cell bodies, it has been proposed that these spikes originate from neurons with cell bodies in layer 2. To address this question, we combined two-photon calcium imaging with electrophysiological recordings from the cortical surface in awake mice using chronically implanted PEDOT:PSS electrode arrays on transparent parylene C substrate. Our electrode arrays (termed Windansee) were integrated with cortical windows offering see-through optical access while also providing measurements of local field potentials (LFP) and multiunit activity (MUA) from the cortical surface. To enable longitudinal data acquisition, we have developed a mechanical solution for installation, connectorization, and protection of Windansee devices aiming for an unhindered access for high numerical aperture microscope objectives and a lifetime of several months while worn by a mouse. Contrary to the common notion, our measurements revealed that only a small fraction of layer 2 neurons from the sampled pool (~13%) faithfully followed MUA recorded from the surface above the imaging field-of-view. Surprised by this result, we turned to computational modeling for an alternative explanation of the MUA signal. Using realistic modeling of neurons with back-propagating dendritic properties, we computed the extracellular action potential at the cortical surface due to firing of local cortical neurons and compared the result to that due to axonal inputs to layer 1. Assuming the literature values for the cell/axon density and firing rates, our modeling results show that surface MUA due to axonal inputs is over an order of magnitude larger than that due to firing of layer 2 pyramidal neurons. Thus, a combination of surface MUA recordings with two-photon calcium imaging can provide complementary information about the input to a cortical column and the local circuit response. Cortical layer I plays an important role in integration of a broad range of cortico-cortical, thalamocortical and neuromodulatory inputs. Therefore, detecting their activity as MUA while combining electrode recording with two-photon imaging using optically transparent surface electrode arrays would facilitate studies of the input/output relationship in cortical circuits, inform computational circuit models, and improve the accuracy of the next generation brain-machine interfaces.

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“…While it is difficult to record spikes directly in peripheral nerves, it is easy to record the LFP generated by nervous activity using surface electrodes. The LFP of a spike volley can be computed using the line-source approximation [28,32]. A typical LFP waveform generated by a single spike is triphasic, with an initial hyperpolarisation, intermediate depolarisation, and final hyperpolarisation.…”

Section: Discussionmentioning

confidence: 99%

Modelling the effect of ephaptic coupling on spike propagation in peripheral nerve fibres

Schmidt

oumlsche

2021

Preprint

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Experimental and theoretical studies have shown that ephaptic coupling leads to the synchronisation and slowing down of spikes propagating along the axons within peripheral nerve bundles. However, the main focus thus far has been on a small number of identical axons, whereas realistic peripheral nerve bundles contain numerous axons with different diameters. Here, we present a computationally efficient spike propagation model, which captures the essential features of propagating spikes and their ephaptic interaction, and facilitates the theoretical investigation of spike volleys in large, heterogeneous fibre bundles. The spike propagation model describes an action potential, or spike, by its position on the axon, and its velocity. The velocity is primarily defined by intrinsic features of the axons, such as diameter and myelination status, but it is also modulated by changes in the extracellular potential. These changes are due to transmembrane currents that occur during the generation of action potentials. The resulting change in the velocity is appropriately described by a linearised coupling function, which is calibrated with a biophysical model. We first lay out the theoretical basis to describe how the spike in an active axon changes the membrane potential of a passive axon. These insights are then incorporated into the spike propagation model, which is calibrated with a biophysically realistic model based on Hodgkin-Huxley dynamics. The fully calibrated model is then applied to fibre bundles with a large number of axons and different types of axon diameter distributions. One key insight of this study is that the heterogeneity of the axonal diameters has a dispersive effect, and that with increasing level of heterogeneity the ephaptic coupling strength has to increase to achieve full synchronisation between spikes. Another result of this study is that in the absence of full synchronisation, a subset of spikes on axons with similar diameter can form synchronised clusters. These findings may help interpret the results of noninvasive experiments on the electrophysiology of peripheral nerves.

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Dipolar extracellular potentials generated by axonal projections

Cited by 3 publications

References 64 publications

Dipolar extracellular potentials generated by axonal projections

Dipolar extracellular potentials generated by axonal projections

Imaging through Windansee electrode arrays reveals a small fraction of local neurons following surface MUA

Modelling the effect of ephaptic coupling on spike propagation in peripheral nerve fibres

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