Common fronto-temporal effective connectivity in humans and monkeys

Neuron. 2021 Mar 3;109(5):852-868.e8. doi: 10.1016/j.neuron.2020.12.026. Epub 2021 Jan 21.

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.

Keywords: cognition; declarative memory; evolution; frontal cortex; hippocampus; language; neural principles; neuroimaging; neurophysiology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Auditory Cortex / physiology
  • Brain Mapping
  • Electric Stimulation
  • Female
  • Frontal Lobe / physiology*
  • Humans
  • Macaca mulatta
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Neural Pathways / physiology
  • Parahippocampal Gyrus / physiology
  • Prefrontal Cortex / physiology
  • Species Specificity
  • Temporal Lobe / physiology*
  • Young Adult