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Articles, Systems/Circuits

Rich-Club Organization in Effective Connectivity among Cortical Neurons

Sunny Nigam, Masanori Shimono, Shinya Ito, Fang-Chin Yeh, Nicholas Timme, Maxym Myroshnychenko, Christopher C. Lapish, Zachary Tosi, Pawel Hottowy, Wesley C. Smith, Sotiris C. Masmanidis, Alan M. Litke, Olaf Sporns and John M. Beggs
Journal of Neuroscience 20 January 2016, 36 (3) 670-684; https://doi.org/10.1523/JNEUROSCI.2177-15.2016
Sunny Nigam
1Department of Physics and
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Masanori Shimono
1Department of Physics and
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Shinya Ito
3Santa Cruz Institute for Particle Physics, University of California at Santa Cruz, Santa Cruz, California 95064,
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Fang-Chin Yeh
4Duke-NUS Graduate Medical School Singapore, Department of Neuroscience and Behavioural Disorders, Singapore 169857,
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Nicholas Timme
1Department of Physics and
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Maxym Myroshnychenko
2Program in Neuroscience, Indiana University, Bloomington, Indiana 47405,
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Christopher C. Lapish
5School of Science Institute for Mathematical Modeling and Computational Sciences, Indiana University-Purdue University, Indianapolis, Indianapolis, Indiana 46202,
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Zachary Tosi
6School of Informatics and Computing, College of Arts and Sciences, and
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Pawel Hottowy
8Physics and Applied Computer Science, AGH University of Science and Technology, 30-059 Krakow, Poland, and
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Wesley C. Smith
9Department of Neurobiology and
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Sotiris C. Masmanidis
10California NanoSystems Institute, University of California, Los Angeles, Los Angeles, California 90095
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Alan M. Litke
4Duke-NUS Graduate Medical School Singapore, Department of Neuroscience and Behavioural Disorders, Singapore 169857,
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Olaf Sporns
7Department of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana 47401,
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John M. Beggs
1Department of Physics and
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Abstract

The performance of complex networks, like the brain, depends on how effectively their elements communicate. Despite the importance of communication, it is virtually unknown how information is transferred in local cortical networks, consisting of hundreds of closely spaced neurons. To address this, it is important to record simultaneously from hundreds of neurons at a spacing that matches typical axonal connection distances, and at a temporal resolution that matches synaptic delays. We used a 512-electrode array (60 μm spacing) to record spontaneous activity at 20 kHz from up to 500 neurons simultaneously in slice cultures of mouse somatosensory cortex for 1 h at a time. We applied a previously validated version of transfer entropy to quantify information transfer. Similar to in vivo reports, we found an approximately lognormal distribution of firing rates. Pairwise information transfer strengths also were nearly lognormally distributed, similar to reports of synaptic strengths. Some neurons transferred and received much more information than others, which is consistent with previous predictions. Neurons with the highest outgoing and incoming information transfer were more strongly connected to each other than chance, thus forming a “rich club.” We found similar results in networks recorded in vivo from rodent cortex, suggesting the generality of these findings. A rich-club structure has been found previously in large-scale human brain networks and is thought to facilitate communication between cortical regions. The discovery of a small, but information-rich, subset of neurons within cortical regions suggests that this population will play a vital role in communication, learning, and memory.

SIGNIFICANCE STATEMENT Many studies have focused on communication networks between cortical brain regions. In contrast, very few studies have examined communication networks within a cortical region. This is the first study to combine such a large number of neurons (several hundred at a time) with such high temporal resolution (so we can know the direction of communication between neurons) for mapping networks within cortex. We found that information was not transferred equally through all neurons. Instead, ∼70% of the information passed through only 20% of the neurons. Network models suggest that this highly concentrated pattern of information transfer would be both efficient and robust to damage. Therefore, this work may help in understanding how the cortex processes information and responds to neurodegenerative diseases.

  • effective connectivity
  • information transfer
  • microcircuits
  • rich club
  • transfer entropy

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The Journal of Neuroscience: 36 (3)
Journal of Neuroscience
Vol. 36, Issue 3
20 Jan 2016
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Rich-Club Organization in Effective Connectivity among Cortical Neurons
Sunny Nigam, Masanori Shimono, Shinya Ito, Fang-Chin Yeh, Nicholas Timme, Maxym Myroshnychenko, Christopher C. Lapish, Zachary Tosi, Pawel Hottowy, Wesley C. Smith, Sotiris C. Masmanidis, Alan M. Litke, Olaf Sporns, John M. Beggs
Journal of Neuroscience 20 January 2016, 36 (3) 670-684; DOI: 10.1523/JNEUROSCI.2177-15.2016

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Rich-Club Organization in Effective Connectivity among Cortical Neurons
Sunny Nigam, Masanori Shimono, Shinya Ito, Fang-Chin Yeh, Nicholas Timme, Maxym Myroshnychenko, Christopher C. Lapish, Zachary Tosi, Pawel Hottowy, Wesley C. Smith, Sotiris C. Masmanidis, Alan M. Litke, Olaf Sporns, John M. Beggs
Journal of Neuroscience 20 January 2016, 36 (3) 670-684; DOI: 10.1523/JNEUROSCI.2177-15.2016
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Keywords

  • effective connectivity
  • information transfer
  • microcircuits
  • rich club
  • transfer entropy

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