Parallel hippocampal-parietal circuits for self- And goal-oriented processing

Annie Zheng; David F. Montez; Scott Marek; Adrian W. Gilmore; Dillan J. Newbold; Timothy O. Laumann; Benjamin P. Kay; Nicole A. Seider; Andrew N. Van; Jacqueline M. Hampton; Dimitrios Alexopoulos; Bradley L. Schlaggar; Chad M. Sylvester; Deanna J. Greene; Joshua S. Shimony; Steven M. Nelson; Gagan S. Wig; Caterina Gratton; Kathleen B. McDermott; Marcus E. Raichle; Evan M. Gordon; Nico U.F. Dosenbach

doi:10.1073/pnas.2101743118

Parallel hippocampal-parietal circuits for self- And goal-oriented processing

Annie Zheng, David F. Montez, Scott Marek, Adrian W. Gilmore, Dillan J. Newbold, Timothy O. Laumann, Benjamin P. Kay, Nicole A. Seider, Andrew N. Van, Jacqueline M. Hampton, Dimitrios Alexopoulos, Bradley L. Schlaggar, Chad M. Sylvester, Deanna J. Greene, Joshua S. Shimony, Steven M. Nelson, Gagan S. Wig, Caterina Gratton, Kathleen B. McDermott, Marcus E. RaichleEvan M. Gordon, Nico U.F. Dosenbach

Clinical Behavioral Neuroscience (Pediatrics)

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

The hippocampus is critically important for a diverse range of cognitive processes, such as episodic memory, prospective memory, affective processing, and spatial navigation. Using individual-specific precision functional mapping of resting-state functional MRI data, we found the anterior hippocampus (head and body) to be preferentially functionally connected to the default mode network (DMN), as expected. The hippocampal tail, however, was strongly preferentially functionally connected to the parietal memory network (PMN), which supports goal-oriented cognition and stimulus recognition. This anterior–posterior dichotomy of resting-state functional connectivity was well-matched by differences in task deactivations and anatomical segmentations of the hippocampus. Task deactivations were localized to the hippocampal head and body (DMN), relatively sparing the tail (PMN). The functional dichotomization of the hippocampus into anterior DMN-connected and posterior PMN-connected parcels suggests parallel but distinct circuits between the hippocampus and medial parietal cortex for self- versus goal-oriented processing.

Original language	English (US)
Article number	e2101743118
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	34
DOIs	https://doi.org/10.1073/pnas.2101743118
State	Published - Aug 24 2021

Bibliographical note

Funding Information:
This work was supported by NIH Grant Nos. NS115672 and MH123091 (A.Z.); NS088590, MH096773, MH124567, MH122066, and MH121276 (N.U.F.D.); MH118370 and pilot funding support from the Northwestern Alzheimer’s Disease Center NIA P30AG13854 (C.G.); MH122389 and MH109983 (C.M.S.); HD087011 (J.S.S.); NS110332 (D.J.N.); and MH121518 (S.M.); and funds provided by the Kiwanis Neuroscience Research Foundation (N.U.F.D.), the Jacobs Foundation (N.U.F.D.), and the McDonnell Center for Systems Neuroscience at Washington University in St. Louis (A.Z., N.U.F.D., and D.J.N).

Funding Information:
ACKNOWLEDGMENTS. This work was supported by NIH Grant Nos. NS115672 and MH123091 (A.Z.); NS088590, MH096773, MH124567, MH122066, and MH121276 (N.U.F.D.); MH118370 and pilot funding support from the North-western Alzheimer’s Disease Center NIA P30AG13854 (C.G.); MH122389 and MH109983 (C.M.S.); HD087011 (J.S.S.); NS110332 (D.J.N.); and MH121518 (S.M.); and funds provided by the Kiwanis Neuroscience Research Foundation (N.U.F.D.), the Jacobs Foundation (N.U.F.D.), and the McDonnell Center for Systems Neuroscience at Washington University in St. Louis (A.Z., N.U.F.D., and D.J.N).

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Keywords

Brain networks
Functional connectivity
Hippocampus
Individual variability
Resting state

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10.1073/pnas.2101743118

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Zheng, A., Montez, D. F., Marek, S., Gilmore, A. W., Newbold, D. J., Laumann, T. O., Kay, B. P., Seider, N. A., Van, A. N., Hampton, J. M., Alexopoulos, D., Schlaggar, B. L., Sylvester, C. M., Greene, D. J., Shimony, J. S., Nelson, S. M., Wig, G. S., Gratton, C., McDermott, K. B., ... Dosenbach, N. U. F. (2021). Parallel hippocampal-parietal circuits for self- And goal-oriented processing. Proceedings of the National Academy of Sciences of the United States of America, 118(34), [e2101743118]. https://doi.org/10.1073/pnas.2101743118

Zheng, A, Montez, DF, Marek, S, Gilmore, AW, Newbold, DJ, Laumann, TO, Kay, BP, Seider, NA, Van, AN, Hampton, JM, Alexopoulos, D, Schlaggar, BL, Sylvester, CM, Greene, DJ, Shimony, JS, Nelson, SM, Wig, GS, Gratton, C, McDermott, KB, Raichle, ME, Gordon, EM & Dosenbach, NUF 2021, 'Parallel hippocampal-parietal circuits for self- And goal-oriented processing', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 34, e2101743118. https://doi.org/10.1073/pnas.2101743118

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title = "Parallel hippocampal-parietal circuits for self- And goal-oriented processing",

abstract = "The hippocampus is critically important for a diverse range of cognitive processes, such as episodic memory, prospective memory, affective processing, and spatial navigation. Using individual-specific precision functional mapping of resting-state functional MRI data, we found the anterior hippocampus (head and body) to be preferentially functionally connected to the default mode network (DMN), as expected. The hippocampal tail, however, was strongly preferentially functionally connected to the parietal memory network (PMN), which supports goal-oriented cognition and stimulus recognition. This anterior–posterior dichotomy of resting-state functional connectivity was well-matched by differences in task deactivations and anatomical segmentations of the hippocampus. Task deactivations were localized to the hippocampal head and body (DMN), relatively sparing the tail (PMN). The functional dichotomization of the hippocampus into anterior DMN-connected and posterior PMN-connected parcels suggests parallel but distinct circuits between the hippocampus and medial parietal cortex for self- versus goal-oriented processing.",

keywords = "Brain networks, Functional connectivity, Hippocampus, Individual variability, Resting state",

author = "Annie Zheng and Montez, {David F.} and Scott Marek and Gilmore, {Adrian W.} and Newbold, {Dillan J.} and Laumann, {Timothy O.} and Kay, {Benjamin P.} and Seider, {Nicole A.} and Van, {Andrew N.} and Hampton, {Jacqueline M.} and Dimitrios Alexopoulos and Schlaggar, {Bradley L.} and Sylvester, {Chad M.} and Greene, {Deanna J.} and Shimony, {Joshua S.} and Nelson, {Steven M.} and Wig, {Gagan S.} and Caterina Gratton and McDermott, {Kathleen B.} and Raichle, {Marcus E.} and Gordon, {Evan M.} and Dosenbach, {Nico U.F.}",

note = "Funding Information: This work was supported by NIH Grant Nos. NS115672 and MH123091 (A.Z.); NS088590, MH096773, MH124567, MH122066, and MH121276 (N.U.F.D.); MH118370 and pilot funding support from the Northwestern Alzheimer{\textquoteright}s Disease Center NIA P30AG13854 (C.G.); MH122389 and MH109983 (C.M.S.); HD087011 (J.S.S.); NS110332 (D.J.N.); and MH121518 (S.M.); and funds provided by the Kiwanis Neuroscience Research Foundation (N.U.F.D.), the Jacobs Foundation (N.U.F.D.), and the McDonnell Center for Systems Neuroscience at Washington University in St. Louis (A.Z., N.U.F.D., and D.J.N). Funding Information: ACKNOWLEDGMENTS. This work was supported by NIH Grant Nos. NS115672 and MH123091 (A.Z.); NS088590, MH096773, MH124567, MH122066, and MH121276 (N.U.F.D.); MH118370 and pilot funding support from the North-western Alzheimer{\textquoteright}s Disease Center NIA P30AG13854 (C.G.); MH122389 and MH109983 (C.M.S.); HD087011 (J.S.S.); NS110332 (D.J.N.); and MH121518 (S.M.); and funds provided by the Kiwanis Neuroscience Research Foundation (N.U.F.D.), the Jacobs Foundation (N.U.F.D.), and the McDonnell Center for Systems Neuroscience at Washington University in St. Louis (A.Z., N.U.F.D., and D.J.N). Publisher Copyright: {\textcopyright} 2021 National Academy of Sciences. All rights reserved.",

year = "2021",

month = aug,

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doi = "10.1073/pnas.2101743118",

language = "English (US)",

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T1 - Parallel hippocampal-parietal circuits for self- And goal-oriented processing

AU - Zheng, Annie

AU - Montez, David F.

AU - Marek, Scott

AU - Gilmore, Adrian W.

AU - Newbold, Dillan J.

AU - Laumann, Timothy O.

AU - Kay, Benjamin P.

AU - Seider, Nicole A.

AU - Van, Andrew N.

AU - Hampton, Jacqueline M.

AU - Alexopoulos, Dimitrios

AU - Schlaggar, Bradley L.

AU - Sylvester, Chad M.

AU - Greene, Deanna J.

AU - Shimony, Joshua S.

AU - Nelson, Steven M.

AU - Wig, Gagan S.

AU - Gratton, Caterina

AU - McDermott, Kathleen B.

AU - Raichle, Marcus E.

AU - Gordon, Evan M.

AU - Dosenbach, Nico U.F.

N1 - Funding Information: This work was supported by NIH Grant Nos. NS115672 and MH123091 (A.Z.); NS088590, MH096773, MH124567, MH122066, and MH121276 (N.U.F.D.); MH118370 and pilot funding support from the Northwestern Alzheimer’s Disease Center NIA P30AG13854 (C.G.); MH122389 and MH109983 (C.M.S.); HD087011 (J.S.S.); NS110332 (D.J.N.); and MH121518 (S.M.); and funds provided by the Kiwanis Neuroscience Research Foundation (N.U.F.D.), the Jacobs Foundation (N.U.F.D.), and the McDonnell Center for Systems Neuroscience at Washington University in St. Louis (A.Z., N.U.F.D., and D.J.N). Funding Information: ACKNOWLEDGMENTS. This work was supported by NIH Grant Nos. NS115672 and MH123091 (A.Z.); NS088590, MH096773, MH124567, MH122066, and MH121276 (N.U.F.D.); MH118370 and pilot funding support from the North-western Alzheimer’s Disease Center NIA P30AG13854 (C.G.); MH122389 and MH109983 (C.M.S.); HD087011 (J.S.S.); NS110332 (D.J.N.); and MH121518 (S.M.); and funds provided by the Kiwanis Neuroscience Research Foundation (N.U.F.D.), the Jacobs Foundation (N.U.F.D.), and the McDonnell Center for Systems Neuroscience at Washington University in St. Louis (A.Z., N.U.F.D., and D.J.N). Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.

PY - 2021/8/24

Y1 - 2021/8/24

N2 - The hippocampus is critically important for a diverse range of cognitive processes, such as episodic memory, prospective memory, affective processing, and spatial navigation. Using individual-specific precision functional mapping of resting-state functional MRI data, we found the anterior hippocampus (head and body) to be preferentially functionally connected to the default mode network (DMN), as expected. The hippocampal tail, however, was strongly preferentially functionally connected to the parietal memory network (PMN), which supports goal-oriented cognition and stimulus recognition. This anterior–posterior dichotomy of resting-state functional connectivity was well-matched by differences in task deactivations and anatomical segmentations of the hippocampus. Task deactivations were localized to the hippocampal head and body (DMN), relatively sparing the tail (PMN). The functional dichotomization of the hippocampus into anterior DMN-connected and posterior PMN-connected parcels suggests parallel but distinct circuits between the hippocampus and medial parietal cortex for self- versus goal-oriented processing.

AB - The hippocampus is critically important for a diverse range of cognitive processes, such as episodic memory, prospective memory, affective processing, and spatial navigation. Using individual-specific precision functional mapping of resting-state functional MRI data, we found the anterior hippocampus (head and body) to be preferentially functionally connected to the default mode network (DMN), as expected. The hippocampal tail, however, was strongly preferentially functionally connected to the parietal memory network (PMN), which supports goal-oriented cognition and stimulus recognition. This anterior–posterior dichotomy of resting-state functional connectivity was well-matched by differences in task deactivations and anatomical segmentations of the hippocampus. Task deactivations were localized to the hippocampal head and body (DMN), relatively sparing the tail (PMN). The functional dichotomization of the hippocampus into anterior DMN-connected and posterior PMN-connected parcels suggests parallel but distinct circuits between the hippocampus and medial parietal cortex for self- versus goal-oriented processing.

KW - Brain networks

KW - Functional connectivity

KW - Hippocampus

KW - Individual variability

KW - Resting state

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

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M1 - e2101743118

ER -

Parallel hippocampal-parietal circuits for self- And goal-oriented processing

Abstract

Bibliographical note

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