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On-line, voluntary control of human temporal lobe neurons

Subjects

Abstract

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.

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Figure 1: Experimental set-up.
Figure 2: Task performance and neuronal spiking.
Figure 3: Successful fading.
Figure 4: Voluntary control at the single unit level.

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Acknowledgements

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).

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Contributions

M.C., F.M., R.Q.Q., C.K. and I.F. designed the experiment; M.C. performed the experiments; I.F. performed the surgeries; M.C. and N.T. analysed the data; M.C., C.K. and I.F. wrote the manuscript. All authors discussed the data and the analysis methods and contributed to the manuscript.

Corresponding authors

Correspondence to Moran Cerf or Christof Koch or Itzhak Fried.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods and Results, Supplementary Figures 1-9 with legends, legends for Supplementary Movie 1 and additional references. (PDF 6206 kb)

Supplementary Movie 1

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)

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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

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