Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Creators: Rocchi, Francesca; Oya, Hiroyuki; Balezeau, Fabien; Billig, Alexander J.; Kocsis, Zsuzsanna; Jenison, Rick L.; Nourski, Kirill V.; Kovach, Christopher K.; Steinschneider, Mitchell; Kikuchi, Yukiko; Rhone, Ariane E.; Dlouhy, Brian J.; Kawasaki, Hiroto; Adolphs, Ralph; Greenlee, Jeremy D. W.; Griffiths, Timothy D.; Howard, Matthew A., III; Petkov, Christopher I.

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.

Additional Information

© 2021 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Received 24 April 2020, Revised 2 October 2020, Accepted 30 December 2020, Available online 21 January 2021. We acknowledge the contribution of the neurosurgery patients and the nonhuman primates in this work. For the human work, we thank H. Chen and P.E. Gander for es-fMRI experiment assistance, M.A. Granner for safety monitoring, V. Magnotta for technical consultation, and J.M. Buatti for help with MRI logistics. For the macaque work, we thank J. Nacef and the Comparative Biology Centre animal technician and veterinary teams. We thank M.I. Banks and P.E. Gander for useful discussion. This work was supported by Wellcome Trust (WT092606AIA; to C.I.P.), European Research Council Horizon 2020 (ERC CoG, Consolidator Grant, MECHIDENT 724198; to C.I.P.), and National Institutes of Health (R01 DC004290-20 to M.A.H.; U01 NS103780-03 to R.A.). The human work was conducted on an MRI instrument funded by National Institutes of Health grant 1S10OD025025-01. Author contributions: Conceptualization and Project Administration, C.I.P., M.A.H., and T.D.G.; Investigation and Formal Analysis, F.R., H.O., Z.K., R.L.J., and C.I.P.; Methodology and Materials, F.R., H.O., F.B., Z.K., R.L.J., K.V.N., C.K.K., M.S., Y.K., A.E.R., B.J.D., H.K., J.D.W.G., M.A.H., and C.I.P.; Writing – Original Draft, C.I.P., F.R., and H.O.; Writing – Review and Editing, C.I.P., F.R., H.O., F.B., A.J.B., Z.K., R.L.J., K.V.N., Y.K., A.E.R., B.J.D., H.K., R.A., J.D.W.G., T.D.G., and M.A.H.; Funding Acquisition, C.I.P., M.A.H., T.D.G., R.A., and J.D.W.G.; Data Curation and Resources, F.R., H.O., and C.I.P. The authors declare no competing interests. Data and code availability: The macaque and human datasets generated during this study are available as follows. For the macaque data: Open Science Framework https://osf.io/arqp8, PRIMatE Data Exchange https://fcon_1000.projects.nitrc.org/indi/indiPRIME.html and PRIMatE Resource Exchange: https://prime-re.github.io/. For the human data: Open Science Framework https://osf.io/arqp8 or Open Neuro https:// openneuro.org/. This study did not generate unique code.

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Supplemental Material - 1-s2.0-S0896627320310308-mmc5.mp4

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