Interindividual Variability of Functional Connectivity in Awake and Anesthetized Rhesus Macaque Monkeys

Ting Xu, Darrick Sturgeon, Julian S.B. Ramirez, Seán Froudist-Walsh, Daniel S. Margulies, Charles E. Schroeder, Damien A. Fair, Michael P. Milham

Research output: Contribution to journalArticlepeer-review

41 Scopus citations

Abstract

Background: Nonhuman primate (NHP)models are commonly used to advance our understanding of brain function and organization. However, to date, they have offered few insights into individual differences among NHPs. In large part, this is due to the logistical challenges of NHP research, which limit most studies to 5 subjects or fewer. Methods: We leveraged the availability of a large-scale open NHP imaging resource to provide an initial examination of individual differences in the functional organization of the NHP brain. Specifically, we selected one awake functional magnetic resonance imaging dataset (Newcastle University: n = 10)and two anesthetized functional magnetic resonance imaging datasets (Oxford University: n = 19; University of California, Davis: n = 19)to examine individual differences in functional connectivity characteristics across the cortex as well as potential state dependencies. Results: We noted significant individual variations of functional connectivity across the macaque cortex. Similar to the findings in humans, during the awake state, the primary sensory and motor cortices showed lower variability than the high-order association regions. This variability pattern was significantly correlated with T1-weighted and T2-weighted mapping and degree of long-distance connectivity, but not short-distance connectivity. The interindividual variability under anesthesia exhibited a very distinct pattern, with lower variability in medial frontal cortex, precuneus, and somatomotor regions and higher variability in the lateral ventral frontal and insular cortices. Conclusions: This work has implications for our understanding of the evolutionary origins of individual variation in the human brain and methodological implications that must be considered in any pursuit to study individual variation in NHP models.

Original languageEnglish (US)
Pages (from-to)543-553
Number of pages11
JournalBiological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume4
Issue number6
DOIs
StatePublished - Jun 2019
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported by gifts from Joseph P. Healey, Phyllis Green, and Randolph Cowen to the Child Mind Institute and the National Institutes of Health (Brain Research through Advancing Innovative Neurotechnologies Initiative Grant Nos. R01-MH111439 [to CES and MPM], P50MH109429 [to CES], R01-MH107508 [to DAF], and P60-AA010760, R01-MH115357, R01-MH096773, and P50-MH100029 [to DAF]), National Institutes of Health (Grant No. P01AG026423), and Yerkes National Primate Research Center Office of Research Infrastructure Programs (Grant No. OD P51OD11132). We thank the investigative teams from Newcastle University (J. Nacef, C.I. Petkov, F. Balezeau, T.D. Griffiths, C. Poirier, A. Thiele, M. Ortiz, M. Schmid, D. Hunter), Oxford University (J. Sallet, R.B. Mars, M.F.S. Rushworth), and University of California, Davis (M.G. Baxter, P.L. Croxson, J.H. Morrison)and the funding agencies that made their work possible (University of California, Davis: National Institute on Aging; Newcastle: National Center for 3Rs, National Institutes of Health, Wellcome Trust, UK Biotechnology Biological Sciences Research Council; Oxford University: Wellcome Trust, Royal Society, Medical Research Council, UK Biotechnology, and Biological Sciences Research Council). The authors report no biomedical financial interests or potential conflicts of interest.

Funding Information:
We thank the investigative teams from Newcastle University (J. Nacef, C.I. Petkov, F. Balezeau, T.D. Griffiths, C. Poirier, A. Thiele, M. Ortiz, M. Schmid, D. Hunter), Oxford University (J. Sallet, R.B. Mars, M.F.S. Rushworth), and University of California, Davis (M.G. Baxter, P.L. Croxson, J.H. Morrison) and the funding agencies that made their work possible ( University of California , Davis: National Institute on Aging; Newcastle: National Center for 3Rs , National Institutes of Health , Wellcome Trust , UK Biotechnology Biological Sciences Research Council ; Oxford University : Wellcome Trust, Royal Society, Medical Research Council, UK Biotechnology, and Biological Sciences Research Council).

Funding Information:
This work was supported by gifts from Joseph P. Healey , Phyllis Green , and Randolph Cowen to the Child Mind Institute and the National Institutes of Health ( Brain Research through Advancing Innovative Neurotechnologies Initiative Grant Nos. R01-MH111439 [to CES and MPM], P50MH109429 [to CES], R01-MH107508 [to DAF], and P60-AA010760 , R01-MH115357 , R01-MH096773 , and P50-MH100029 [to DAF]), National Institutes of Health (Grant No. P01AG026423 ), and Yerkes National Primate Research Center Office of Research Infrastructure Programs (Grant No. OD P51OD11132 ).

Funding Information:
This work was supported by gifts from Joseph P. Healey, Phyllis Green, and Randolph Cowen to the Child Mind Institute and the National Institutes of Health (Brain Research through Advancing Innovative Neurotechnologies Initiative Grant Nos. R01-MH111439 [to CES and MPM], P50MH109429 [to CES], R01-MH107508 [to DAF], and P60-AA010760, R01-MH115357, R01-MH096773, and P50-MH100029 [to DAF]), National Institutes of Health (Grant No. P01AG026423), and Yerkes National Primate Research Center Office of Research Infrastructure Programs (Grant No. OD P51OD11132). We thank the investigative teams from Newcastle University (J. Nacef, C.I. Petkov, F. Balezeau, T.D. Griffiths, C. Poirier, A. Thiele, M. Ortiz, M. Schmid, D. Hunter), Oxford University (J. Sallet, R.B. Mars, M.F.S. Rushworth), and University of California, Davis (M.G. Baxter, P.L. Croxson, J.H. Morrison) and the funding agencies that made their work possible (University of California, Davis: National Institute on Aging; Newcastle: National Center for 3Rs, National Institutes of Health, Wellcome Trust, UK Biotechnology Biological Sciences Research Council; Oxford University: Wellcome Trust, Royal Society, Medical Research Council, UK Biotechnology, and Biological Sciences Research Council). The authors report no biomedical financial interests or potential conflicts of interest.

Publisher Copyright:
© 2019 Society of Biological Psychiatry

Keywords

  • Anesthesia
  • Awake
  • Functional connectivity
  • Interindividual variation
  • Nonhuman primate
  • fMRI

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