Daily life continually confronts us with an exuberance of external, sensory stimuli competing with a rich stream of internal deliberations, plans and ruminations. The brain must select one or more of these for further processing. How this competition is resolved across multiple sensory and cognitive regions is not known; nor is it clear how internal thoughts and attention regulate this competition1,2,3,4. Recording from single neurons in patients implanted with intracranial electrodes for clinical reasons5,6,7,8,9, here we demonstrate that humans can regulate the activity of their neurons in the medial temporal lobe (MTL) to alter the outcome of the contest between external images and their internal representation. Subjects looked at a hybrid superposition of two images representing familiar individuals, landmarks, objects or animals and had to enhance one image at the expense of the other, competing one. Simultaneously, the spiking activity of their MTL neurons in different subregions and hemispheres was decoded in real time to control the content of the hybrid. Subjects reliably regulated, often on the first trial, the firing rate of their neurons, increasing the rate of some while simultaneously decreasing the rate of others. They did so by focusing onto one image, which gradually became clearer on the computer screen in front of their eyes, and thereby overriding sensory input. On the basis of the firing of these MTL neurons, the dynamics of the competition between visual images in the subject’s mind was visualized on an external display.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Chalupa, L., Werner, J. & Barnstable, C. The Visual Neurosciences (MIT Press, 2004)
Thorpe, S. Single units and sensation: still just as relevant today. Perception 38, 804–807 (2009)
Blake D. A. R., ed. Binocular Rivalry (MIT Press, 2005)
Reynolds, J. & Chelazzi, L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 27, 611–648 (2004)
Quian Quiroga, R. et al. Explicit encoding of multimodal percepts by single neurons in the human brain. Curr. Biol. 19, 1308–1313 (2009).
Quian Quiroga, R. et al. Invariant visual representation by single neurons in the human brain. Nature 435, 1102–1107 (2005)
Földiák, P. Neural coding: non-local but explicit and conceptual. Curr. Biol. 19, R904–R906 (2009)
Kreiman, G., Koch, C. & Fried, I. Imagery neurons in the human brain. Nature 408, 357–361 (2000)
Gelbard-Sagiv, H. et al. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322, 96–101 (2008)
Reddy, L., Kanwisher, N. & VanRullen, R. Attention and biased competition in multi-voxel object representations. Proc. Natl Acad. Sci. USA 106, 21447–21452 (2009)
Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995)
Serences, J. et al. Control of object-based attention in human cortex. Cereb. Cortex 14, 1346–1357 (2004)
Fried, I., MacDonald, K. & Wilson, C. Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 18, 753–765 (1997)
Quian Quiroga, R. et al. Decoding visual inputs from multiple neurons in the human temporal lobe. J. Neurophysiol. 98, 1997–2007 (2007)
Musallam, S. et al. Cognitive control signals for neural prosthetics. Science 305, 258–262 (2004)
Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361–365 (2000)
Velliste, M. et al. Cortical control of a prosthetic arm for self-feeding. Nature 453, 1098–1101 (2008)
Moritz, C., Perlmutter, S. & Fetz, E. Direct control of paralysed muscles by cortical neurons. Nature 456, 639–642 (2008)
Hochberg, L. et al. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442, 164–171 (2006)
Kim, S. et al. Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia. J. Neural Eng. 5, 455–476 (2008)
Kennedy, P. et al. Direct control of a computer from the human central nervous system. IEEE Trans. Rehabil. Eng. 8, 198–202 (2000)
Guenther, F. et al. A wireless brain-machine interface for real-time speech synthesis. PLoS ONE 4, e8218 (2009)
Waydo, S. et al. Sparse representation in the human medial temporal lobe. J. Neurosci. 26, 10232–10234 (2006)
We thank the patients for their participation in these studies. We thank K. Laird, A. Postolova, N. Parikshak and V. Isiaka for help with the recordings; E. Behnke and T. Fields for technical support; G. Mulliken and U. Rutishauser for comments on the manuscript; and M. Moon for help with data visualization. This work was supported by grants from the National Institute of Neurological Disorders and Stroke (NINDS), the National Institute of Mental Health (NIMH), the G. Harold & Leila Y. Mathers Charitable Foundation, and the WCU programme through the National Research Foundation of Korea funded by the Ministry of Education, Science and Technology (R31-2008-000-10008-0).
The authors declare no competing financial interests.
This file contains Supplementary Methods and Results, Supplementary Figures 1-9 with legends, legends for Supplementary Movie 1 and additional references. (PDF 6206 kb)
An example of a feedback experiment, this movie has three parts. The first part shows the control presentation, part two shows a sequence of trials from the actual experiment and part three shows the 16 Monroe Brolin trials in the order they appeared in the experiment - see Supplementary Information file for full legend. (MP4 12778 kb)
About this article
Cite this article
Cerf, M., Thiruvengadam, N., Mormann, F. et al. On-line, voluntary control of human temporal lobe neurons. Nature 467, 1104–1108 (2010). https://doi.org/10.1038/nature09510
Neural Computation (2021)
Operant conditioning of motor cortex neurons reveals neuron-subtype-specific responses in a brain-machine interface task
Scientific Reports (2020)
Connection Science (2020)
Trends in Cognitive Sciences (2020)