Increased hippocampal-prefrontal functional connectivity in insomnia

Jeanne Leerssen, Rick Wassing, Jennifer R Ramautar, Diederick Stoffers, Oti Lakbila-Kamal, Joy Perrier, Jessica Bruijel, Jessica C Foster-Dingley, Moji Aghajani, Eus J W van Someren

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Insomnia Disorder (ID) is the second-most common mental disorder and has a far-reaching impact on daytime functioning. A meta-analysis indicates that, of all cognitive domains, declarative memory involving the hippocampus is most affected in insomnia. Hippocampal functioning has consistently been shown to be sensitive to experimental sleep deprivation. Insomnia however differs from sleep deprivation in many aspects, and findings on hippocampal structure and function have been equivocal. The present study used both structural and resting-state functional Magnetic Resonance Imaging in a larger sample than previously reported to evaluate hippocampal volume and functional connectivity in ID. Included were 65 ID patients (mean age = 48.3 y ± 14.0, 17 males) and 65 good sleepers (mean age = 44.1 y ± 15.2, 23 males). Insomnia severity was assessed with the Insomnia Severity Index (ISI), subjective sleep with the Consensus Sleep Diary (CSD) and objective sleep by two nights of polysomnography (PSG). Seed-based analysis showed a significantly stronger connectivity of the bilateral hippocampus with the left middle frontal gyrus in ID than in controls (p = .035, cluster based correction for multiple comparisons). Further analyses across all participants moreover showed that individual differences in the strength of this connectivity were associated with insomnia severity (ISI, r = 0.371, p = 9.3e-5) and with subjective sleep quality (CSD sleep efficiency, r = -0.307, p = .009) (all p FDR-corrected). Hippocampal volume did not differ between ID and controls. The findings indicate more severe insomnia and worse sleep quality in people with a stronger functional connectivity between the bilateral hippocampus and the left middle frontal gyrus, part of a circuit that characteristically activates with maladaptive rumination and deactivates with sleep.

Original languageEnglish
JournalNeurobiology of Learning and Memory
DOIs
Publication statusE-pub ahead of print - 12 Feb 2018

Cite this

Leerssen, Jeanne ; Wassing, Rick ; Ramautar, Jennifer R ; Stoffers, Diederick ; Lakbila-Kamal, Oti ; Perrier, Joy ; Bruijel, Jessica ; Foster-Dingley, Jessica C ; Aghajani, Moji ; van Someren, Eus J W. / Increased hippocampal-prefrontal functional connectivity in insomnia. In: Neurobiology of Learning and Memory. 2018.
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title = "Increased hippocampal-prefrontal functional connectivity in insomnia",
abstract = "Insomnia Disorder (ID) is the second-most common mental disorder and has a far-reaching impact on daytime functioning. A meta-analysis indicates that, of all cognitive domains, declarative memory involving the hippocampus is most affected in insomnia. Hippocampal functioning has consistently been shown to be sensitive to experimental sleep deprivation. Insomnia however differs from sleep deprivation in many aspects, and findings on hippocampal structure and function have been equivocal. The present study used both structural and resting-state functional Magnetic Resonance Imaging in a larger sample than previously reported to evaluate hippocampal volume and functional connectivity in ID. Included were 65 ID patients (mean age = 48.3 y ± 14.0, 17 males) and 65 good sleepers (mean age = 44.1 y ± 15.2, 23 males). Insomnia severity was assessed with the Insomnia Severity Index (ISI), subjective sleep with the Consensus Sleep Diary (CSD) and objective sleep by two nights of polysomnography (PSG). Seed-based analysis showed a significantly stronger connectivity of the bilateral hippocampus with the left middle frontal gyrus in ID than in controls (p = .035, cluster based correction for multiple comparisons). Further analyses across all participants moreover showed that individual differences in the strength of this connectivity were associated with insomnia severity (ISI, r = 0.371, p = 9.3e-5) and with subjective sleep quality (CSD sleep efficiency, r = -0.307, p = .009) (all p FDR-corrected). Hippocampal volume did not differ between ID and controls. The findings indicate more severe insomnia and worse sleep quality in people with a stronger functional connectivity between the bilateral hippocampus and the left middle frontal gyrus, part of a circuit that characteristically activates with maladaptive rumination and deactivates with sleep.",
author = "Jeanne Leerssen and Rick Wassing and Ramautar, {Jennifer R} and Diederick Stoffers and Oti Lakbila-Kamal and Joy Perrier and Jessica Bruijel and Foster-Dingley, {Jessica C} and Moji Aghajani and {van Someren}, {Eus J W}",
note = "Copyright {\circledC} 2018 Elsevier Inc. All rights reserved.",
year = "2018",
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day = "12",
doi = "10.1016/j.nlm.2018.02.006",
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Leerssen, J, Wassing, R, Ramautar, JR, Stoffers, D, Lakbila-Kamal, O, Perrier, J, Bruijel, J, Foster-Dingley, JC, Aghajani, M & van Someren, EJW 2018, 'Increased hippocampal-prefrontal functional connectivity in insomnia' Neurobiology of Learning and Memory. https://doi.org/10.1016/j.nlm.2018.02.006

Increased hippocampal-prefrontal functional connectivity in insomnia. / Leerssen, Jeanne; Wassing, Rick; Ramautar, Jennifer R; Stoffers, Diederick; Lakbila-Kamal, Oti; Perrier, Joy; Bruijel, Jessica; Foster-Dingley, Jessica C; Aghajani, Moji; van Someren, Eus J W.

In: Neurobiology of Learning and Memory, 12.02.2018.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Increased hippocampal-prefrontal functional connectivity in insomnia

AU - Leerssen, Jeanne

AU - Wassing, Rick

AU - Ramautar, Jennifer R

AU - Stoffers, Diederick

AU - Lakbila-Kamal, Oti

AU - Perrier, Joy

AU - Bruijel, Jessica

AU - Foster-Dingley, Jessica C

AU - Aghajani, Moji

AU - van Someren, Eus J W

N1 - Copyright © 2018 Elsevier Inc. All rights reserved.

PY - 2018/2/12

Y1 - 2018/2/12

N2 - Insomnia Disorder (ID) is the second-most common mental disorder and has a far-reaching impact on daytime functioning. A meta-analysis indicates that, of all cognitive domains, declarative memory involving the hippocampus is most affected in insomnia. Hippocampal functioning has consistently been shown to be sensitive to experimental sleep deprivation. Insomnia however differs from sleep deprivation in many aspects, and findings on hippocampal structure and function have been equivocal. The present study used both structural and resting-state functional Magnetic Resonance Imaging in a larger sample than previously reported to evaluate hippocampal volume and functional connectivity in ID. Included were 65 ID patients (mean age = 48.3 y ± 14.0, 17 males) and 65 good sleepers (mean age = 44.1 y ± 15.2, 23 males). Insomnia severity was assessed with the Insomnia Severity Index (ISI), subjective sleep with the Consensus Sleep Diary (CSD) and objective sleep by two nights of polysomnography (PSG). Seed-based analysis showed a significantly stronger connectivity of the bilateral hippocampus with the left middle frontal gyrus in ID than in controls (p = .035, cluster based correction for multiple comparisons). Further analyses across all participants moreover showed that individual differences in the strength of this connectivity were associated with insomnia severity (ISI, r = 0.371, p = 9.3e-5) and with subjective sleep quality (CSD sleep efficiency, r = -0.307, p = .009) (all p FDR-corrected). Hippocampal volume did not differ between ID and controls. The findings indicate more severe insomnia and worse sleep quality in people with a stronger functional connectivity between the bilateral hippocampus and the left middle frontal gyrus, part of a circuit that characteristically activates with maladaptive rumination and deactivates with sleep.

AB - Insomnia Disorder (ID) is the second-most common mental disorder and has a far-reaching impact on daytime functioning. A meta-analysis indicates that, of all cognitive domains, declarative memory involving the hippocampus is most affected in insomnia. Hippocampal functioning has consistently been shown to be sensitive to experimental sleep deprivation. Insomnia however differs from sleep deprivation in many aspects, and findings on hippocampal structure and function have been equivocal. The present study used both structural and resting-state functional Magnetic Resonance Imaging in a larger sample than previously reported to evaluate hippocampal volume and functional connectivity in ID. Included were 65 ID patients (mean age = 48.3 y ± 14.0, 17 males) and 65 good sleepers (mean age = 44.1 y ± 15.2, 23 males). Insomnia severity was assessed with the Insomnia Severity Index (ISI), subjective sleep with the Consensus Sleep Diary (CSD) and objective sleep by two nights of polysomnography (PSG). Seed-based analysis showed a significantly stronger connectivity of the bilateral hippocampus with the left middle frontal gyrus in ID than in controls (p = .035, cluster based correction for multiple comparisons). Further analyses across all participants moreover showed that individual differences in the strength of this connectivity were associated with insomnia severity (ISI, r = 0.371, p = 9.3e-5) and with subjective sleep quality (CSD sleep efficiency, r = -0.307, p = .009) (all p FDR-corrected). Hippocampal volume did not differ between ID and controls. The findings indicate more severe insomnia and worse sleep quality in people with a stronger functional connectivity between the bilateral hippocampus and the left middle frontal gyrus, part of a circuit that characteristically activates with maladaptive rumination and deactivates with sleep.

U2 - 10.1016/j.nlm.2018.02.006

DO - 10.1016/j.nlm.2018.02.006

M3 - Article

JO - Neurobiology of Learning and Memory

JF - Neurobiology of Learning and Memory

SN - 1074-7427

ER -

Leerssen J, Wassing R, Ramautar JR, Stoffers D, Lakbila-Kamal O, Perrier J et al. Increased hippocampal-prefrontal functional connectivity in insomnia. Neurobiology of Learning and Memory. 2018 Feb 12. https://doi.org/10.1016/j.nlm.2018.02.006