Common fronto-temporal effective connectivity in humans and monkeys

Francesca Rocchi; Hiroyuki Oya; Fabien Balezeau; Alexander J Billig; Zsuzsanna Kocsis; Rick L 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:10.1016/j.neuron.2020.12.026

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Common fronto-temporal effective connectivity in humans and monkeys

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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 L Jenison, Kirill V Nourski, Christopher K Kovach, Mitchell Steinschneider, Yukiko Kikuchi, …

Neuron (Cambridge, Mass.), Vol.109(5), pp.852-868.e8

03/03/2021

DOI: 10.1016/j.neuron.2020.12.026

PMID: 33482086

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Abstract

Human brain pathways supporting language and declarative memory are thought to have differentiated substantially during evolution. However, cross-species comparisons are missing on site-specific effective connectivity between regions important for cognition. We harnessed functional imaging to visualize the effects of direct electrical brain stimulation in macaque monkeys and human neurosurgery patients. We discovered comparable effective connectivity between caudal auditory cortex and both ventro-lateral prefrontal cortex (VLPFC, including area 44) and parahippocampal cortex in both species. Human-specific differences were clearest in the form of stronger hemispheric lateralization effects. In humans, electrical tractography revealed remarkably rapid evoked potentials in VLPFC following auditory cortex stimulation and speech sounds drove VLPFC, consistent with prior evidence in monkeys of direct auditory cortex projections to homologous vocalization-responsive regions. The results identify a common effective connectivity signature in human and nonhuman primates, which from auditory cortex appears equally direct to VLPFC and indirect to the hippocampus. [Display omitted] [Display omitted] •Privileged human auditory to ventral prefrontal connectivity, paralleled in monkeys•Common auditory to parahippocampal effective connectivity in both species•Stronger lateralization of connectivity effects in humans than in monkeys•Human fronto-temporal network rooted in conserved organizational principle Interconnectivity between brain regions crucial for language and declarative memory is thought to have substantially evolutionarily differentiated in humans. Rocchi, Oya and colleagues visualize site-specific brain connectivity in monkeys and human neurosurgery patients. They discover a common neural organizational principle that bridges gaps between primates as neurobiological models and human patients.

Evolution

Neuroimaging

Neurophysiology

frontal cortex

cognition

hippocampus

language

neural principles

declarative memory

Details

Title: Subtitle: Common fronto-temporal effective connectivity in humans and monkeys
Creators: Francesca Rocchi - Biosciences Institute, Newcastle University Medical School, Newcastle upon Tyne, UK
Hiroyuki Oya - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Fabien Balezeau - Biosciences Institute, Newcastle University Medical School, Newcastle upon Tyne, UK
Alexander J Billig - Ear Institute, University College London, London, UK
Zsuzsanna Kocsis - Biosciences Institute, Newcastle University Medical School, Newcastle upon Tyne, UK
Rick L Jenison - Department of Neuroscience, University of Wisconsin - Madison, Madison, WI, USA
Kirill V Nourski - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Christopher K Kovach - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Mitchell Steinschneider - Departments of Neurology and Neuroscience, Albert Einstein College of Medicine, Bronx, NY, USA
Yukiko Kikuchi - Biosciences Institute, Newcastle University Medical School, Newcastle upon Tyne, UK
Ariane E Rhone - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Brian J Dlouhy - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Hiroto Kawasaki - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Ralph Adolphs - Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA
Jeremy D.W Greenlee - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Timothy D Griffiths - Biosciences Institute, Newcastle University Medical School, Newcastle upon Tyne, UK
Matthew A Howard - Department of Neurosurgery, The University of Iowa, Iowa City, IA, USA
Christopher I Petkov - Biosciences Institute, Newcastle University Medical School, Newcastle upon Tyne, UK
Resource Type: Journal article
Publication Details: Neuron (Cambridge, Mass.), Vol.109(5), pp.852-868.e8
DOI: 10.1016/j.neuron.2020.12.026
PMID: 33482086
NLM abbreviation: Neuron
ISSN: 0896-6273
eISSN: 1097-4199
Publisher: Elsevier Inc
Grant note: DOI: 10.13039/501100000781, name: European Research Council; DOI: 10.13039/100000002, name: National Institutes of Health; DOI: 10.13039/100010269, name: Wellcome Trust
Language: English
Date published: 03/03/2021
Academic Unit: Neurology; Stead Family Department of Pediatrics; Psychological and Brain Sciences; Iowa Neuroscience Institute; Neurosurgery; Otolaryngology
Record Identifier: 9984070258202771

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