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Functional neuroanatomy of the human eye movement network: a review and atlas

  • Benjamin Coiner
  • Hong Pan
  • Monica L. Bennett
  • Yelena G. Bodien
  • Swathi Iyer
  • Therese M. O’Neil-Pirozzi
  • Lorene Leung
  • Joseph T. Giacino
  • Emily SternEmail author
Practical Guide

Abstract

The human eye movement network is a complex system that requires the integration of sensory, motor, attentional, and executive processes. Here, we review the neuroanatomy of the eye movement network with an emphasis on functional neuroimaging applications. We consolidate the literature into a concise resource designed to be immediately accessible and applicable to diverse research interests, and present the novel Functional Oculomotor System (FOcuS) Atlas—a tool in stereotaxic space that will simplify and standardize the inclusion of the eye movement network in future functional neuroimaging studies. We anticipate this review and the FOcuS Atlas will facilitate increased examination of the eye movement network across disciplines leading to a thorough understanding of how eye movement network function contributes to higher-order cognition and how it is integrated with other brain networks. Furthermore, functional examination of the eye movement network in patient populations offers the potential for deeper insight into the role of eye movement circuitry in functional network activity, diagnostic assessments, and the indications for augmentative communication systems that rely on eye movement control.

Keywords

Ocular motility Visual processing Eye movement MRI Atlas Network connectivity 

Abbreviations

EMN

Eye movement network

FOcuS

Functional Oculomotor System (Atlas)

Notes

Acknowledgements

We thank Xiao Da (Brigham and Women’s Hospital, Harvard Medical School) for assistance in programming to generate the final version of the Functional Oculomotor System (FOcuS) Atlas in MNI stereotaxic space.

Funding

This work was supported by the National Institute on Disability, Independent Living, and Rehabilitation Research (NIDILRR Grant number 90DP0039). NIDILRR is a Center within the Administration for Community Living (ACL), Department of Health and Human Services (HHS). The contents of this manuscript do not necessarily represent the policy of NIDILRR, ACL, HHS, and you should not assume endorsement by the Federal Government. Additional support was provided by the James S. McDonnell Foundation (Understanding Human Cognition-Collaborative).

Compliance with ethical standards

Conflict of interest

Yelena G. Bodien has received financial support from the James S. McDonnell Foundation, NIH-National Institute on Neurological Disorders and Stroke, and National Institute for Neurologic Disorders and Stroke (NINDS) for Transforming Research. Joseph T. Giacino is a member of the American Congress of Rehabilitation Medicine (ACRM), the Brain Injury Special Interest Group, and the Disorders of Consciousness Task Force; serves on a scientific advisory board for TBI Model Systems National Data and Statistical Center; has received funding for travel from the US Department of Defense for a meeting related to the TBI Endpoint Development Project, the National Institute on Neurological Disorders and Stroke for the Traumatic Brain Injury Model Systems Project Directors meeting, and for a meeting related to the Transforming Research and Clinical Knowledge in Traumatic Brain Injury study, the National Institute on Disability, Independent Living and Rehabilitation Research, the American Academy of Physical Medicine and Rehabilitation, the One Mind Foundation, the James S. McDonnell Foundation for a meeting related to the Recovery of Consciousness After Severe Brain Injury study, the Barbara Epstein Foundation, and the International Brain Injury Association; has received a cash donation from the Epstein Foundation for a hospital clinical program that he directs and for serving on a team that provided clinical consultation services to an overseas patient who sustained severe brain injury; has served as an editor for the Journal of Head Trauma Rehabilitation; has received honoraria from the One Mind Foundation, Holy Cross Hospital (Surrey, UK); HealthSouth Braintree Hospital, Western Michigan Brain Injury Network, George Washington University Medical School, Association of Academic Physiatrists, Mayo Clinic, Kennedy-Krieger Institute, and Magill’s Medical Guide; performs clinical procedures as 10% of his clinical effort in his role as Director of Spaulding Rehabilitation Network Disorders of Consciousness Program and neuroimaging as a PI on 2 neuroimaging studies for 30% of his research effort; received financial support from the NIH-National Institute on Neurological Disorders and Stroke (NINDS) for Central Thalamic Stimulation for Traumatic Brain Injury, U. S. Department of Defense for TBI Endpoint Development Project, the Huperzine A for the Treatment of Cognitive, Mood and Functional Deficits After Moderate and Severe TBI study, the INjury and TRaumatic STress (INTRuST) Consortium Neuroimaging Acquisition and Archival study, the National Institute on Disability, Independent Living and Rehabilitation Research (NIDILRR) for the Spaulding-Harvard Traumatic Brain Injury Model System and for Multicenter Evaluation of Memory Remediation after traumatic Brain Injury with Donepezil, National Institute for Neurologic Disorders and Stroke (NINDS) for Transforming Research and Clinical Knowledge in Traumatic Brain Injury study, James S. McDonnell Foundation for Study of Recovery of Consciousness After Severe Brain Injury, Barbara Epstein Foundation, and the Spaulding Rehabilitation Hospital Department of Physical Medicine and Rehabilitation; and has acted as a witness with regard to a legal proceeding. Emily Stern served as Co-Editor of the International Journal of Imaging Systems and Technology—Neuroimaging and Brain Mapping and serves on the Editorial Board of the Journal of Neuroimaging. She has received funding for travel from the National Institutes of Health and the James S. McDonnell Foundation. She has received an honorarium from the American Academy of Physical Medicine and Rehabilitation and reimbursement for service from the National Institutes of Health. She has three patents submitted: System and Method for z-Shim Compensated Echo-Planar Magnetic Resonance Imaging, and Systems (issued), Methods for Generating Biomarkers Based on Multivariate Classification of Functional Imaging and Associated Data (issued), and System and Method for a Multivariate, Automated, Systematic and Hierarchical Searching Algorithm for Biosignature Extraction and Biomarker Discovery via Task-based fMRI Imaging Spacetime Data. Dr. Stern has received research funding support from the DHSS Administration for Community Living, formerly the National Institute on Disability and Rehabilitation Research (NIDRR—90DP0039-03-01), the Epilepsy Foundation, the NIH (NIMH—R01MH090291, co-investigator), Northeastern University, Gilead Pharmaceutical, Merck Pharmaceutical, and Blackthorn Therapeutics. Dr. Stern is the co-founder and CEO of a startup company, Compass Neurosciences, that will be spinning out of Brigham and Women’s Hospital in the near future. This has not yet occurred, the company presently has no assets, and this activity did not influence what was written in this manuscript. The remaining authors declare that they have no conflict of interest.

Research involving human participants and/or animals and informed consent

This manuscript does not report on any findings from studies that enrolled human participants or animals. Rather, it synthesizes information gathered from existing literature and presents a novel atlas based upon this.

Supplementary material

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Supplementary material 1 (DOCX 57 kb)
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Supplementary material 2 (ZIP 794 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Benjamin Coiner
    • 1
    • 2
    • 3
  • Hong Pan
    • 1
    • 2
  • Monica L. Bennett
    • 1
    • 2
  • Yelena G. Bodien
    • 2
    • 4
    • 5
  • Swathi Iyer
    • 1
    • 2
    • 6
  • Therese M. O’Neil-Pirozzi
    • 5
    • 7
  • Lorene Leung
    • 1
    • 2
    • 8
  • Joseph T. Giacino
    • 2
    • 5
  • Emily Stern
    • 1
    • 2
    • 9
    Email author
  1. 1.Department of PsychiatryBrigham and Women’s HospitalBostonUSA
  2. 2.Harvard Medical SchoolBostonUSA
  3. 3.Eskind Family Biomedical Library and Learning CenterVanderbilt University School of MedicineNashvilleUSA
  4. 4.Department of Neurology, Center for Neurotechnology and NeurorecoveryMassachusetts General HospitalBostonUSA
  5. 5.Department of Physical Medicine and RehabilitationSpaulding Rehabilitation HospitalCharlestownUSA
  6. 6.The MathWorks, IncNatickUSA
  7. 7.Department of Communication Sciences and DisordersNortheastern UniversityBostonUSA
  8. 8.Boston University School of MedicineBostonUSA
  9. 9.Department of RadiologyBrigham and Women’s HospitalBostonUSA

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