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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Rieke, F., Warland, D., de Ruyter Van Steveninck, R. R. & Bialek, W. Spikes: Exploring the Neural Code (MIT Press, Cambridge, Massachusetts, 1997)
Britten, K. H., Newsome, W. T., Shadlen, M. N., Celebrini, S. & Movshon, J. A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996)
Afraz, S. R., Kiani, R. & Esteky, H. Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695 (2006)
Salzman, C. D., Britten, K. H. & Newsome, W. T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990)
Murasugi, C. M., Salzman, C. D. & Newsome, W. T. Microstimulation in visual area MT: effects of varying pulse amplitude and frequency. J. Neurosci. 13, 1719–1729 (1993)
Tehovnik, E. J. Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Methods 65, 1–17 (1996)
Zilles, K. & Wree, A. in The Rat Nervous System (ed. Paxinos, G.) 649–685 (Academic Press, London, 1995)
Beaulieu, C. Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res. 609, 284–292 (1993)
Penfield, W. & Rasmussen, T. The Cerebral Cortex of Man: A Clinical Study of Localization of Function (Macmillan, New York, 1950)
Romo, R., Hernandez, A., Zainos, A. & Salinas, E. Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390 (1998)
Krauss, A., Manns, I. D. & Brecht, M. in Annu. Meeting Soc. Neurosci. 58.19. (2003)
Schmidt, E. M. et al. Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. Brain 119, 507–522 (1996)
Bartlett, J. R. & Doty, R. W. An exploration of the ability of macaques to detect microstimulation of striate cortex. Acta Neurobiol. Exp. (Wars.) 40, 713–727 (1980)
Pinault, D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J. Neurosci. Methods 65, 113–136 (1996)
Talwar, S. K. & Gerstein, G. L. Auditory frequency discrimination in the white rat. Hear. Res. 126, 135–150 (1998)
Swadlow, H. A. Monitoring the excitability of neocortical efferent neurons to direct activation by extracellular current pulses. J. Neurophysiol. 68, 605–619 (1992)
de Kock, C. P., Bruno, R. M., Spors, H. & Sakmann, B. Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. (Lond.) 581, 139–154 (2007)
Stuttgen, M. C., Ruter, J. & Schwarz, C. Two psychophysical channels of whisker deflection in rats align with two neuronal classes of primary afferents. J. Neurosci. 26, 7933–7941 (2006)
Kerr, J. N., Greenberg, D. & Helmchen, F. Imaging input and output of neocortical networks in vivo . Proc. Natl Acad. Sci. USA 102, 14063–14068 (2005)
Margrie, T. W., Brecht, M. & Sakmann, B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 444, 491–498 (2002)
Waters, J. & Helmchen, F. Background synaptic activity is sparse in neocortex. J. Neurosci. 26, 8267–8277 (2006)
Brecht, M. & Sakmann, B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J. Physiol. (Lond.) 543, 49–70 (2002)
Moore, C. I. & Nelson, S. B. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80, 2882–2892 (1998)
Olshausen, B. A. & Field, D. J. Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 14, 481–487 (2004)
Warren, R. A. & Dykes, R. W. Population analysis of single neurons in cat somatosensory cortex. Somatosens. Mot. Res. 9, 297–312 (1992)
DeFelipe, J. & Farinas, I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39, 563–607 (1992)
Song, S., Sjostrom, P. J., Reigl, M., Nelson, S. & Chklovskii, D. B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68 (2005)
Gold, J. I. & Shadlen, M. N. Representation of a perceptual decision in developing oculomotor commands. Nature 404, 390–394 (2000)
Vallbo, A. B., Olsson, K. A., Westberg, K. G. & Clark, F. J. Microstimulation of single tactile afferents from the human hand. Sensory attributes related to unit type and properties of receptive fields. Brain 107, 727–749 (1984)
Brecht, M., Schneider, M., Sakmann, B. & Margrie, T. W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704–710 (2004)
Connors, B. W. & Gutnick, M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99–104 (1990)
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.
Author information
Authors and Affiliations
Corresponding authors
Supplementary information
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)
Rights and permissions
About this article
Cite this article
Houweling, A., Brecht, M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451, 65–68 (2008). https://doi.org/10.1038/nature06447
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature06447
This article is cited by
-
Propagation of activity through the cortical hierarchy and perception are determined by neural variability
Nature Neuroscience (2023)
-
SmaRT2P: a software for generating and processing smart line recording trajectories for population two-photon calcium imaging
Brain Informatics (2022)
-
Local circuit amplification of spatial selectivity in the hippocampus
Nature (2022)
-
Neuronal hyperexcitability in Alzheimer’s disease: what are the drivers behind this aberrant phenotype?
Translational Psychiatry (2022)
-
Emerging imaging methods to study whole-brain function in rodent models
Translational Psychiatry (2021)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.