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

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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. Video Abstract: [Figure presented] 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.

Original languageEnglish (US)
Pages (from-to)852-868.e8
JournalNeuron
Volume109
Issue number5
DOIs
StatePublished - Mar 3 2021

Keywords

  • cognition
  • declarative memory
  • evolution
  • frontal cortex
  • hippocampus
  • language
  • neural principles
  • neuroimaging
  • neurophysiology

ASJC Scopus subject areas

  • Neuroscience(all)

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