Abstract

Cortical surface recording techniques such as EEG and ECoG are widely used for measuring brain activity. The prevailing assumption is that surface potentials primarily reflect synaptic activity, although non-synaptic events may also contribute. Here we show that dendritic calcium spikes occurring in pyramidal neurons (that we showed previously are cognitively relevant) are clearly detectable in cortical surface potentials. To show this we developed an optogenetic, non-synaptic approach to evoke dendritic calcium spikes in vivo. We found that optogenetically evoked calcium spikes were easily detectable and had an unexpected waveform near the cortical surface. Sensory-evoked dendritic calcium spikes were also clearly detectable with amplitudes that matched the contribution of synaptic input. These results reveal how dendritic calcium spikes appear at the cortical surface and their significant impact on surface potentials, suggesting that long-standing surface recording data may contain information about dendritic activity that is relevant to behavior and cognitive function.

Highlights

  • Cortical surface recording techniques such as EEG and ECoG are widely used for measuring brain activity

  • Functional significance, and proximity to the cortical surface, it remains unclear how dendritic spikes contribute to surface potentials, it has been observed that dendritic spikes can influence the local field potential (LFP)[7, 10, 14, 15]

  • We chose a second method for evoking dendritic Ca2+ spikes based on the “critical frequency” approach that uses high-frequency backpropagating action potentials generated at the soma[18, 19]

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Summary

Introduction

Cortical surface recording techniques such as EEG and ECoG are widely used for measuring brain activity. Sensory-evoked dendritic calcium spikes were clearly detectable with amplitudes that matched the contribution of synaptic input These results reveal how dendritic calcium spikes appear at the cortical surface and their significant impact on surface potentials, suggesting that long-standing surface recording data may contain information about dendritic activity that is relevant to behavior and cognitive function. Voltagegated calcium (Ca2+) channels around the main bifurcation point of apical dendrites (550–900 μm from the soma in rats8) give rise to characteristic depolarizing plateau potentials (dendritic Ca2+ spikes)[9] These dendritic Ca2+ spikes can be generated spontaneously or by sensory inputs[10], last for 50 ms in anesthetized animals[8] and up to several seconds in awake behaving rats[11], and represent a large current source[12]. We sought to determine the extent to which dendritic Ca2+ spikes contribute to the surface potentials through combined use of multi-channel extracellular recordings, optogenetics, pharmacology, and a “micro-periscope” that allows layer-specific light delivery

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