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Behavioural report of single neuron stimulation in somatosensory cortex

Abstract

Understanding how neural activity in sensory cortices relates to perception is a central theme of neuroscience. Action potentials of sensory cortical neurons can be strongly correlated to properties of sensory stimuli1 and reflect the subjective judgements of an individual about stimuli2. Microstimulation experiments have established a direct link from sensory activity to behaviour3,4, suggesting that small neuronal populations can influence sensory decisions5. However, microstimulation does not allow identification and quantification of the stimulated cellular elements6. The sensory impact of individual cortical neurons therefore remains unknown. Here we show that stimulation of single neurons in somatosensory cortex affects behavioural responses in a detection task. We trained rats to respond to microstimulation of barrel cortex at low current intensities. We then initiated short trains of action potentials in single neurons by juxtacellular stimulation. Animals responded significantly more often in single-cell stimulation trials than in catch trials without stimulation. Stimulation effects varied greatly between cells, and on average in 5% of trials a response was induced. Whereas stimulation of putative excitatory neurons led to weak biases towards responding, stimulation of putative inhibitory neurons led to more variable and stronger sensory effects. Reaction times for single-cell stimulation were long and variable. Our results demonstrate that single neuron activity can cause a change in the animal’s detection behaviour, suggesting a much sparser cortical code for sensations than previously anticipated.

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Figure 1: Behavioural setup and single-cell stimulation.
Figure 2: Behavioural responses to stimulation of a single layer 5b pyramidal neuron.
Figure 3: Initiation of action potentials in single barrel cortex neurons causes biases towards responding.
Figure 4: Reaction times for single-cell stimulation are long and variable compared with microstimulation responses.

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Acknowledgements

We thank B. Sakmann for suggesting the juxtacellular stimulation approach, J. van der Burg, E. Haasdijk and G. Maas for technical contributions, P. den Iseger and A. Lee for discussions, and G. Borst, M. Frens, C. Hansel, L. Herfst, A. Lee, B. Voigt and J. Wolfe for comments on the manuscript. This work was supported by the Bernstein Center for Computational Neuroscience and Humboldt University Berlin, Erasmus MC, and VIDI (NWO) and HFSP grants to M.B.

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Correspondence to Arthur R. Houweling or Michael Brecht.

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Supplementary Information

This file contains Supplementary Figures S1-S8 with Legends illustrating additional analysis of single cell stimulation experiments in somatosensory cortex. (PDF 496 kb)

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Houweling, A., Brecht, M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451, 65–68 (2008). https://doi.org/10.1038/nature06447

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