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Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Francesca Rocchi, Hiroyuki Oya, Fabien Balezeau, Alexander J. Billig, Zsuzsanna Kocsis, Rick Jenison, Kirill V. Nourski, Christopher K. Kovach, Mitchell Steinschneider, Yukiko Kikuchi, Ariane E. Rhone, Brian J. Dlouhy, Hiroto Kawasaki, Ralph Adolphs, Jeremy D.W. Greenlee, Timothy D. Griffiths, Matthew A. Howard, Christopher I. Petkov
doi: https://doi.org/10.1101/2020.04.03.024042
Francesca Rocchi
1Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne, UK
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  • For correspondence: chris.petkov@ncl.ac.uk hiroyuki-oya@uiowa.edu checca.r1@gmail.com
Hiroyuki Oya
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
7Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, USA
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  • For correspondence: chris.petkov@ncl.ac.uk hiroyuki-oya@uiowa.edu checca.r1@gmail.com
Fabien Balezeau
1Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne, UK
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Alexander J. Billig
3Ear Institute, University College London, UK
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Zsuzsanna Kocsis
1Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne, UK
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Rick Jenison
6Department of Psychology, University of Wisconsin - Madison, Madison, WI, USA
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Kirill V. Nourski
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
7Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, USA
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Christopher K. Kovach
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Mitchell Steinschneider
5Department of Neurology, Albert Einstein College of Medicine, Bronx, NY, USA
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Yukiko Kikuchi
1Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne, UK
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Ariane E. Rhone
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
7Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, USA
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Brian J. Dlouhy
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
7Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, USA
8Pappajohn Biomedical Institute, University of Iowa, Iowa City, IA, USA
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Hiroto Kawasaki
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Ralph Adolphs
4Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA
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Jeremy D.W. Greenlee
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Timothy D. Griffiths
1Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne, UK
3Ear Institute, University College London, UK
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Matthew A. Howard
2Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
7Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, USA
8Pappajohn Biomedical Institute, University of Iowa, Iowa City, IA, USA
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Christopher I. Petkov
1Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne, UK
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  • For correspondence: chris.petkov@ncl.ac.uk hiroyuki-oya@uiowa.edu checca.r1@gmail.com
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ABSTRACT

Cognitive pathways supporting human language and declarative memory are thought to have uniquely evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-specific effective connectivity between regions important for cognition. We harnessed a new approach using functional imaging to visualize the impact of direct electrical brain stimulation in human neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory cortex to vocalization responsive regions in vlPFC. The results identify a common effective connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the hippocampus (via parahippocampal cortex) in human and nonhuman primates.

Highlights

  • Privileged human auditory to inferior frontal connectivity, linked to monkeys

  • Common auditory to parahippocampal effective connectivity in both species

  • Greater lateralization in human effective connectivity, more symmetrical in monkeys

  • Human fronto-temporal network function rooted in evolutionarily conserved signature

eTOC short summary Functional connectivity between regions crucial for language and declarative memory is thought to have substantially differentiated in humans. Using a new technique to similarly visualize directional effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns in both species between fronto-temporal regions crucial for cognition.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 05, 2020.
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Common Fronto-temporal Effective Connectivity in Humans and Monkeys
Francesca Rocchi, Hiroyuki Oya, Fabien Balezeau, Alexander J. Billig, Zsuzsanna Kocsis, Rick Jenison, Kirill V. Nourski, Christopher K. Kovach, Mitchell Steinschneider, Yukiko Kikuchi, Ariane E. Rhone, Brian J. Dlouhy, Hiroto Kawasaki, Ralph Adolphs, Jeremy D.W. Greenlee, Timothy D. Griffiths, Matthew A. Howard, Christopher I. Petkov
bioRxiv 2020.04.03.024042; doi: https://doi.org/10.1101/2020.04.03.024042
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Common Fronto-temporal Effective Connectivity in Humans and Monkeys
Francesca Rocchi, Hiroyuki Oya, Fabien Balezeau, Alexander J. Billig, Zsuzsanna Kocsis, Rick Jenison, Kirill V. Nourski, Christopher K. Kovach, Mitchell Steinschneider, Yukiko Kikuchi, Ariane E. Rhone, Brian J. Dlouhy, Hiroto Kawasaki, Ralph Adolphs, Jeremy D.W. Greenlee, Timothy D. Griffiths, Matthew A. Howard, Christopher I. Petkov
bioRxiv 2020.04.03.024042; doi: https://doi.org/10.1101/2020.04.03.024042

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