Shared and distinct contributions of rostrolateral prefrontal cortex to analogical reasoning and episodic memory retrieval

Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mecha...

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Published inHuman brain mapping Vol. 37; no. 3; pp. 896 - 912
Main Authors Westphal, Andrew J., Reggente, Nicco, Ito, Kaori L., Rissman, Jesse
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.03.2016
John Wiley & Sons, Inc
John Wiley and Sons Inc
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Abstract Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom‐up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi‐voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto‐parietal control network across tasks, its coupling with other cortical areas varied in a task‐dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain‐general role for left RLPFC in monitoring and/or integrating task‐relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations. Hum Brain Mapp 37:896–912, 2016. © 2015 Wiley Periodicals, Inc.
AbstractList Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom-up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi-voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto-parietal control network across tasks, its coupling with other cortical areas varied in a task-dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain-general role for left RLPFC in monitoring and/or integrating task-relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations. Hum Brain Mapp 37:896-912, 2016. © 2015 Wiley Periodicals, Inc.
Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom‐up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi‐voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto‐parietal control network across tasks, its coupling with other cortical areas varied in a task‐dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain‐general role for left RLPFC in monitoring and/or integrating task‐relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations. Hum Brain Mapp 37:896–912, 2016 . © 2015 Wiley Periodicals, Inc .
Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom-up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi-voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto-parietal control network across tasks, its coupling with other cortical areas varied in a task-dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain-general role for left RLPFC in monitoring and/or integrating task-relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations. Hum Brain Mapp 37:896-912, 2016. copyright 2015 Wiley Periodicals, Inc.
Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom-up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi-voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto-parietal control network across tasks, its coupling with other cortical areas varied in a task-dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain-general role for left RLPFC in monitoring and/or integrating task-relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations.
Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom-up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi-voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto-parietal control network across tasks, its coupling with other cortical areas varied in a task-dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain-general role for left RLPFC in monitoring and/or integrating task-relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations.Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory retrieval. However, these tasks have typically been studied in isolation, and thus it is unclear whether they involve common or distinct RLPFC mechanisms. Here, we introduce a novel functional magnetic resonance imaging (fMRI) task paradigm to compare brain activity during reasoning and memory tasks while holding bottom-up perceptual stimulation and response demands constant. Univariate analyses on fMRI data from twenty participants identified a large swath of left lateral prefrontal cortex, including RLPFC, that showed common engagement on reasoning trials with valid analogies and memory trials with accurately retrieved source details. Despite broadly overlapping recruitment, multi-voxel activity patterns within left RLPFC reliably differentiated these two trial types, highlighting the presence of at least partially distinct information processing modes. Functional connectivity analyses demonstrated that while left RLPFC showed consistent coupling with the fronto-parietal control network across tasks, its coupling with other cortical areas varied in a task-dependent manner. During the memory task, this region strengthened its connectivity with the default mode and memory retrieval networks, whereas during the reasoning task it coupled more strongly with a nearby left prefrontal region (BA 45) associated with semantic processing, as well as with a superior parietal region associated with visuospatial processing. Taken together, these data suggest a domain-general role for left RLPFC in monitoring and/or integrating task-relevant knowledge representations and showcase how its function cannot solely be attributed to episodic memory or analogical reasoning computations.
Author Westphal, Andrew J.
Rissman, Jesse
Ito, Kaori L.
Reggente, Nicco
AuthorAffiliation 3 Brain Research Institute, University of California Los Angeles Los Angeles California
4 Integrative Center for Learning and Memory, University of California Los Angeles Los Angeles California
1 Department of Psychology University of California Los Angeles Los Angeles California
2 Department of Psychiatry and Biobehavioral Sciences University of California Los Angeles Los Angeles California
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relational integration
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source memory
functional connectivity
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rostral prefrontal cortex
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Braver TS, Reynolds JR, Donaldson DI (2003): Neural mechanisms of transient and sustained cognitive control during task switching. Neuron 39:713-726.
Green AE, Fugelsang JA, Kraemer DJM, Shamosh NA, Dunbar KN (2006): Frontopolar cortex mediates abstract integration in analogy. Brain Res 1096:125-137.
Dobbins IG, Wagner AD (2005): Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. Cereb Cortex 15:1768-1778.
Koechlin E, Basso G, Pietrini P, Panzer S, Grafman J (1999): The role of the anterior prefrontal cortex in human cognition. Nature 399:148-151.
Ramnani N, Owen AM (2004): Anterior prefrontal cortex: Insights into function from anatomy and neuroimaging. Nat Rev Neurosci 5:184-194.
Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997): Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6:218-229.
Christoff K, Keramatian K, Gordon AM, Smith R, Madler B (2009): Prefrontal organization of cognitive control according to levels of abstraction. Brain Res 1286:94-105.
Goldberg RF, Perfetti CA, Fiez JA, Schneider W (2007): Selective retrieval of abstract semantic knowledge in left prefrontal cortex. J Neurosci 27:3790-3798.
Simons JS, Henson RNA, Gilbert SJ, Fletcher PC (2008): Separable forms of reality monitoring supported by the anterior prefrontal cortex. J Cogn Neurosci 20:447-457.
Beck SM, Ruge H, Walser M, Goschke T (2014): The functional neuroanatomy of spontaneous retrieval and strategic monitoring of delayed intentions. Neuropsychologia 52:37-50.
Christoff K, Prabhakaran V, Dorfman J, Zhao Z, Kroger JK, Holyoak KJ, Gabrieli JDE (2001): Rostrolateral prefrontal cortex involvement in relational integration during reasoning. NeuroImage 14:1136-1149.
Wagner AD, Paré-Blagoev EJ, Clark J, Poldrack RA (2001): Recovering meaning: left prefrontal cortex guides controlled semantic retrieval. Neuron 31:329-338.
Davis T, LaRocque KF, Mumford JA, Norman KA, Wagner AD, Poldrack RA (2014): What do differences between multi-voxel and univariate analysis mean? How subject-, voxel-, and trial-level variance impact fMRI analysis. NeuroImage 97:271-283.
Spreng RN, Stevens WD, Chamberlain JP, Gilmore AW, Schacter DL (2010): Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. NeuroImage 53:303-317.
Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2012): Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22:158-165.
Christoff K, Ream JM, Geddes LPT, Gabrieli JDE (2003): Evaluating self-generated information: Anterior prefrontal contributions to human cognition. Behav Neurosci 117:1161-1168.
Burgess PW, Gonen-Yaacovi G, Volle E (2011): Functional neuroimaging studies of prospective memory: What have we learnt so far? Neuropsychologia 49:2246-2257.
Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007): Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104:11073-11078.
Ranganath C, Johnson MK, D'Esposito M (2000): Left anterior prefrontal activation increases with demands to recall specific perceptual information. J Neurosci 20:19-57.
Tong F, Pratte MS (2012): Decoding patterns of human brain activity. Annu Rev Psychol 63:483-509.
Kennedy DN, Lange N, Makris N, Bates J, Meyer J, Caviness VS (1998): Gyri of the human neocortex: an MRI-based analysis of volume and variance. Cereb Cortex 8:372-384.
Bunge SA, Wendelken C (2009): Comparing the bird in the hand with the ones in the bush. Neuron 62:609-611.
Momennejad I, Haynes J (2012): Human anterior prefrontal cortex encodes the 'what' and 'when'of future intentions. Neuroimage 61:139-148.
Gilbert SJ, Frith CD, Burgess PW (2005): Involvement of rostral prefrontal cortex in selection between stimulus-oriented and stimulus-independent thought. Eur. J. Neurosci 21:1423-1431.
Pereira F, Mitchell T, Botvinick M (2009): Machine learning classifiers and fMRI: A tutorial overview. Neuroimage 45:S199-S209.
Badre D, D'Esposito M (2007): Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J Cogn Neurosci 19:2082-2099.
Anwander A, Tittgemeyer M, von Cramon DY, Friederici AD, Knösche TR (2007): Connectivity-based parcellation of Broca's area. Cereb Cortex 17:816-825.
Sakai K, Passingham RE (2002): Prefrontal interactions reflect future task operations. Nat Neurosci 6:75-81.
Duncan J, Owen AM (2000): Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475-483.
Jimura K, Poldrack RA (2012): Analyses of regional-average activation and multivoxel pattern information tell complementary stories. Neuropsychologia 50:544-552.
Vendetti MS, Bunge SA (2014): Evolutionary and developmental changes in the lateral frontoparietal network: A little goes a long way for higher-level cognition. Neuron 84:906-917.
Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann TO, Miezin FM, Schlaggar BL (2011): Functional network organization of the human brain. Neuron 72:665-678.
Charron S, Koechlin E (2010): Divided representation of concurrent goals in the human frontal lobes. Science 328:360-363.
Gilbert SJ, Gonen-Yaacovi G, Benoit RG, Volle E, Burgess PW (2010): Distinct functional connectivity associated with lateral versus medial rostral prefrontal cortex: A meta-analysis. Neuroimage 53:1359-1367.
Worsley KJ, Taylor JE, Tomaiuolo F, Lerch J (2004): Unified univariate and multivariate random field theory. NeuroImage 23:189.
Rissman J, Wagner AD (2012): Distributed representations in memory: Insights from functional brain imaging. Annu Rev Psychol 63:101-128.
Bunge SA, Wendelken C, Badre D, Wagner AD (2005): Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms. Cereb Cortex 15:239-249.
Todd MT, Nystrom LE, Cohen JD (2013): Confounds in multivariate pattern analysis: Theory and rule representation case study. NeuroImage 77:157-165.
Badre D, D'Esposito M (2009): Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci 10:659-669.
Petersen SE, Dubis JW (2012): The mixed block/event-related design. Neuroimage 62:1177-1184.
Koechlin E, Ody C, Kouneiher F (2003): The architecture of cognitive control in the human prefrontal cortex. Science 302:1181-1185.
Wendelken C, Chung D, Bunge SA (2012): Rostrolateral prefrontal cortex: Domain-general or domain-sensitive? Hum. Brain Mapp 33:1952-1963.
Lepage M, Ghaffar O, Nyberg L, Tulving E (2000): Prefrontal cortex and episodic memory retrieval mode. Proc Natl Acad Sci USA 97:506-511.
Krawczyk DC (2012): The cognition and neuroscience of relational reasoning. Brain Res 1428:13-23.
Kriegeskorte N, Goebel R, Bandettini P (2006): Information-based functional brain mapping. Proc Natl Acad Sci USA 103:3863-3868.
Gilbert SJ (2011): Decoding the content of delayed intentions. J Neurosci 31:2888-2894.
Cabeza R, Nyberg L (2000): Imaging cognition II: An empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12:1-47.
Volle E, Gilbert SJ, Benoit RG, Burgess PW (2010): Specialization of the rostral prefrontal cortex for distinct analogy processes. Cereb Cortex 20:2647-2659.
Rissman J, Greely HT, Wagner AD (2010): Detecting individual memories through the neural decoding of memory states and past experience. Proc Natl Acad Sci USA 107:9849-9854.
Wagner AD, Shannon BJ, Kahn I, Buckner RL (2005): Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 9:445-453.
Bunge SA, Helskog EH, Wendelken C (2009): Left, but not right, rostrolateral prefrontal cortex meets a stringent test of the relational integration hypothesis. NeuroImage 46:338-342.
Wendelken C, Bunge SA, Carter CS (2008a): Maintaining structured information: An investigation into functions of parietal and lateral prefrontal cortices. Neuropsychologia 46:665-678.
Visscher KM, Miezin FM, Kelly JE, Buckner RL, Donaldson DI, McAvoy MP, Bhalodia VM, Petersen SE (2003): Mixed blocked/event-related designs separate transient and sustained activity in fMRI. NeuroImage 19:1694-1708.
Menon V, Uddin LQ (2010): Saliency, switching, attention and control: A network model of insula function. Brain Struct Funct 214:655-667.
Dobbins IG, Han S (2006): Cue-versus probe-dependent prefrontal cortex activity during contextual remembering. J Cogn Neurosci 18:1439-1452.
Van Essen DC (2005): A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28:635-662.
Cho S, Moody TD, Fernandino L, Mumford JA, Poldrack RA, Cannon TD, Knowlton BJ, Holyoak KJ (2010): Common and dissociable prefrontal loci associated with component mechanisms of analogical reasoning. Cereb Cortex 20:524-533.
Christoff K, Gabrieli JDE (2000): The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology 28:168-186.
Ciaramelli E, Grady CL, Moscovitch M (2008): Top-down and bottom-up attention to memory: A hypothesis (AtoM) on the role of th
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  start-page: 239
  year: 2005
  end-page: 249
  article-title: Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms
  publication-title: Cereb Cortex
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  start-page: 1136
  year: 2001
  end-page: 1149
  article-title: Rostrolateral prefrontal cortex involvement in relational integration during reasoning
  publication-title: NeuroImage
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  start-page: 506
  year: 2000
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SSID ssj0011501
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Snippet Rostrolateral prefrontal cortex (RLPFC) is widely appreciated to support higher cognitive functions, including analogical reasoning and episodic memory...
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SourceType Open Access Repository
Aggregation Database
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Enrichment Source
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StartPage 896
SubjectTerms Adult
Brain Mapping
Cerebrovascular Circulation - physiology
Cognition - physiology
decoding
Female
functional connectivity
Functional Laterality
Humans
Magnetic Resonance Imaging
Male
Memory, Episodic
Multivariate Analysis
multivariate pattern classification
network analysis
Neural Pathways - physiology
Neuropsychological Tests
Oxygen - blood
Perception - physiology
Prefrontal Cortex - physiology
relational integration
rostral prefrontal cortex
semantic
Semantics
source memory
Thinking - physiology
Young Adult
Title Shared and distinct contributions of rostrolateral prefrontal cortex to analogical reasoning and episodic memory retrieval
URI https://api.istex.fr/ark:/67375/WNG-8T56V9M3-2/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhbm.23074
https://www.ncbi.nlm.nih.gov/pubmed/26663572
https://www.proquest.com/docview/1763732396
https://www.proquest.com/docview/1764697876
https://www.proquest.com/docview/1776666630
https://pubmed.ncbi.nlm.nih.gov/PMC6867376
Volume 37
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