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Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control.
J Neurosci 2019; 39(31):6180-6189JN

Abstract

Recent theoretical advances have motivated the hypothesis that the periaqueductal gray (PAG) participates in behaviors that involve changes in the autonomic control of visceromotor activity, including during cognitively demanding tasks. We used ultra-high-field (7 tesla) fMRI to measure human brain activity at 1.1 mm resolution while participants completed a working memory task. Consistent with prior work, participants were less accurate and responded more slowly with increasing memory load-signs of increasing task difficulty. Whole-brain fMRI analysis revealed increased activity in multiple cortical areas with increasing working memory load, including frontal and parietal cortex, dorsal cingulate, supplementary motor area, and anterior insula. Several dopamine-rich midbrain nuclei, such as the substantia nigra and ventral tegmental area, also exhibited load-dependent increases in activation. To investigate PAG involvement during cognitive engagement, we developed an automated method for segmenting and spatially normalizing the PAG. Analyses using cross-validated linear support vector machines showed that the PAG discriminated high versus low working memory load conditions with 95% accuracy in individual subjects based on activity increases in lateral and ventrolateral PAG. Effect sizes in the PAG were comparable in magnitude to those in many of the cortical areas. These findings suggest that cognitive control is not only associated with cortical activity in the frontal and parietal lobes, but also with increased activity in the subcortical PAG and other midbrain regions involved in the regulation of autonomic nervous system function.SIGNIFICANCE STATEMENT Functional neuroimaging in humans has shown that cognitive control engages multiple corticostriatal networks and brainstem nuclei, but theoretical advances suggest that the periaqueductal gray (PAG) should also be engaged during cognitively demanding tasks. Recent advances in ultra-high-field fMRI provided an opportunity to obtain the first evidence that increased activation of intermediate and rostral portions of lateral and ventrolateral PAG columns in humans is modulated by cognitive load. These findings suggest that cognitive control is not solely mediated by activity in the cortex, but that midbrain structures important for autonomic regulation also play a crucial role in higher-order cognition.

Authors+Show Affiliations

Department of Psychology and Neuroscience and the Institute of Cognitive Science, philip.kragel@colorado.edu a.satpute@northeastern.edu. Institute for Behavioral Genetics, University of Colorado, Boulder 80309.Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129.Department of Psychology, Northeastern University, Boston, Massachusetts 02115.Department of Psychology and Neuroscience and the Institute of Cognitive Science.Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129.Department of Psychology, Northeastern University, Boston, Massachusetts 02115. Center for Healthcare Organization and Implementation Research (CHOIR) and the Social and Community Reintegration Research Program (SoCRR), Edith Nourse Rogers Memorial VA Hospital, Bedford, Massachusetts 01730.Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129.Department of Psychology and Neuroscience and the Institute of Cognitive Science.Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129. Department of Psychology, Northeastern University, Boston, Massachusetts 02115. Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114, and.Department of Psychology, Northeastern University, Boston, Massachusetts 02115, philip.kragel@colorado.edu a.satpute@northeastern.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31160537

Citation

Kragel, Philip A., et al. "Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 39, no. 31, 2019, pp. 6180-6189.
Kragel PA, Bianciardi M, Hartley L, et al. Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control. J Neurosci. 2019;39(31):6180-6189.
Kragel, P. A., Bianciardi, M., Hartley, L., Matthewson, G., Choi, J. K., Quigley, K. S., ... Satpute, A. B. (2019). Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 39(31), pp. 6180-6189. doi:10.1523/JNEUROSCI.2043-18.2019.
Kragel PA, et al. Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control. J Neurosci. 2019 Jul 31;39(31):6180-6189. PubMed PMID: 31160537.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control. AU - Kragel,Philip A, AU - Bianciardi,Marta, AU - Hartley,Ludger, AU - Matthewson,Gordon, AU - Choi,Ji-Kyung, AU - Quigley,Karen S, AU - Wald,Lawrence L, AU - Wager,Tor D, AU - Feldman Barrett,Lisa, AU - Satpute,Ajay B, Y1 - 2019/06/03/ PY - 2019/02/18/received PY - 2019/05/22/revised PY - 2019/05/28/accepted PY - 2020/01/31/pmc-release PY - 2019/6/5/pubmed PY - 2019/6/5/medline PY - 2019/6/5/entrez KW - allostasis KW - cognitive control KW - fMRI KW - periaqueductal gray KW - working memory SP - 6180 EP - 6189 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 39 IS - 31 N2 - Recent theoretical advances have motivated the hypothesis that the periaqueductal gray (PAG) participates in behaviors that involve changes in the autonomic control of visceromotor activity, including during cognitively demanding tasks. We used ultra-high-field (7 tesla) fMRI to measure human brain activity at 1.1 mm resolution while participants completed a working memory task. Consistent with prior work, participants were less accurate and responded more slowly with increasing memory load-signs of increasing task difficulty. Whole-brain fMRI analysis revealed increased activity in multiple cortical areas with increasing working memory load, including frontal and parietal cortex, dorsal cingulate, supplementary motor area, and anterior insula. Several dopamine-rich midbrain nuclei, such as the substantia nigra and ventral tegmental area, also exhibited load-dependent increases in activation. To investigate PAG involvement during cognitive engagement, we developed an automated method for segmenting and spatially normalizing the PAG. Analyses using cross-validated linear support vector machines showed that the PAG discriminated high versus low working memory load conditions with 95% accuracy in individual subjects based on activity increases in lateral and ventrolateral PAG. Effect sizes in the PAG were comparable in magnitude to those in many of the cortical areas. These findings suggest that cognitive control is not only associated with cortical activity in the frontal and parietal lobes, but also with increased activity in the subcortical PAG and other midbrain regions involved in the regulation of autonomic nervous system function.SIGNIFICANCE STATEMENT Functional neuroimaging in humans has shown that cognitive control engages multiple corticostriatal networks and brainstem nuclei, but theoretical advances suggest that the periaqueductal gray (PAG) should also be engaged during cognitively demanding tasks. Recent advances in ultra-high-field fMRI provided an opportunity to obtain the first evidence that increased activation of intermediate and rostral portions of lateral and ventrolateral PAG columns in humans is modulated by cognitive load. These findings suggest that cognitive control is not solely mediated by activity in the cortex, but that midbrain structures important for autonomic regulation also play a crucial role in higher-order cognition. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/31160537/Functional_involvement_of_human_periaqueductal_gray_and_other_midbrain_nuclei_in_cognitive_control L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=31160537 DB - PRIME DP - Unbound Medicine ER -