The effects of electrical microstimulation on cortical signal propagation

Abstract

Electrical stimulation has been used in animals and humans to study potential causal links between neural activity and specific cognitive functions. Recently, it has found increasing use in electrotherapy and neural prostheses. However, the manner in which electrical stimulation–elicited signals propagate in brain tissues remains unclear. We used combined electrostimulation, neurophysiology, microinjection and functional magnetic resonance imaging (fMRI) to study the cortical activity patterns elicited during stimulation of cortical afferents in monkeys. We found that stimulation of a site in the lateral geniculate nucleus (LGN) increased the fMRI signal in the regions of primary visual cortex (V1) that received input from that site, but suppressed it in the retinotopically matched regions of extrastriate cortex. Consistent with previous observations, intracranial recordings indicated that a short excitatory response occurring immediately after a stimulation pulse was followed by a long-lasting inhibition. Following microinjections of GABA antagonists in V1, LGN stimulation induced positive fMRI signals in all of the cortical areas. Taken together, our findings suggest that electrical stimulation disrupts cortico-cortical signal propagation by silencing the output of any neocortical area whose afferents are electrically stimulated.

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Figure 1: Effects of thalamic microstimulation on the primary and extrastriate cortices.
Figure 2: Sequential or combined visual and electrical stimulation of the LGN (anesthetized animal B06, session B06fu1).
Figure 3: Population BOLD responses to visual stimulation and electrical stimulation of LGN and pulvinar.
Figure 4: Single-session and population responses to electrical stimulation in alert monkeys.
Figure 5: Effects of stimulation frequency on the BOLD responses (session B06td1).
Figure 6: Typical multiunit responses in V1 to electrical stimulation of LGN.
Figure 7: Analysis of population data.

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Acknowledgements

We thank C. Kayser, O. Eschenko and M. Munk for reading the manuscript and for useful suggestions. Many thanks also go to D. Blaurock for editing, S. Weber for fine-mechanic work and T. Steudel and P. Douay for help with the alert monkey experiments. This research was supported by the Max Planck Society, the German Research Foundation (DFG SFB-A9) and by the intramural research program of the US National Institutes of Health (National Institute Neurological Disorders and Stroke, H.M.).

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N.K.L. conceived the project, designed and supervised the experiments under anesthesia, analyzed the data and wrote the paper. M.A. and Y.M. conducted the experiments. A.R. designed and conducted the pharmacology experiments. F.S. helped with flat-map reconstructions. J.G. and Y.M. conducted the alert monkey experiments. A.O. developed and optimized the data acquisition and microstimulation hardware. H.M. developed and optimized the radiofrequency coils.

Corresponding author

Correspondence to Nikos K Logothetis.

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The authors declare no competing financial interests.

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Logothetis, N., Augath, M., Murayama, Y. et al. The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 13, 1283–1291 (2010). https://doi.org/10.1038/nn.2631

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