Medial temporal lobe functional network architecture supports sleep-related emotional memory processing in older adults

Miranda G Chappel-Farley; Jenna N Adams; Richard F Betzel; John C Janecek; Negin S Sattari; Destiny E Berisha; Novelle J Meza; Hamid Niknazar; Soyun Kim; Abhishek Dave; Ivy Y Chen; Kitty K Lui; Ariel B Neikrug; Ruth M Benca; Michael A Yassa; Bryce A Mander

doi:10.1101/2023.10.27.564260

Medial temporal lobe functional network architecture supports sleep-related emotional memory processing in older adults

bioRxiv [Preprint]. 2023 Nov 1:2023.10.27.564260. doi: 10.1101/2023.10.27.564260.

Authors

Miranda G Chappel-Farley^{1

2}, Jenna N Adams^{1

2}, Richard F Betzel³, John C Janecek^{1

2}, Negin S Sattari⁴, Destiny E Berisha^{1

2}, Novelle J Meza^{1

2}, Hamid Niknazar⁵, Soyun Kim^{1

2}, Abhishek Dave^{5

4}, Ivy Y Chen⁴, Kitty K Lui⁶, Ariel B Neikrug⁴, Ruth M Benca^{1

2

4

7

8

9

10}, Michael A Yassa^{1

2

4

10

11}, Bryce A Mander^{2

5

4

10

12}

Affiliations

¹ Department of Neurobiology and Behavior, University of California Irvine, Irvine CA, 92697, USA.
² Center for the Neurobiology of Learning and Memory, University of California Irvine, Irvine CA, 92697, USA.
³ Department of Psychological and Brain Sciences, University of Indiana Bloomington, Bloomington IN, 47405.
⁴ Department of Psychiatry and Human Behavior, University of California Irvine, Irvine CA, 92697, USA.
⁵ Department of Cognitive Sciences, University of California Irvine, Irvine CA, 92697, USA.
⁶ San Diego State University/University of California San Diego, Joint Doctoral Program in Clinical Psychology, San Diego, CA, 92093, USA.
⁷ Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, 53706, USA.
⁸ Department of Psychiatry, University of Wisconsin-Madison, Madison, 53706, WI, USA.
⁹ Department of Psychiatry and Behavioral Medicine, Wake Forest University, Winston-Salem, NC, 27109, USA.
¹⁰ Institute for Memory Impairments and Neurological Disorders, University of California Irvine, Irvine CA, 92697, USA.
¹¹ Department of Neurology, University of California Irvine, Irvine CA, 92697, USA.
¹² Department of Pathology and Laboratory Medicine, University of California Irvine, Irvine CA, 92697, USA.

Abstract

Memory consolidation occurs via reactivation of a hippocampal index during non-rapid eye movement slow-wave sleep (NREM SWS) which binds attributes of an experience existing within cortical modules. For memories containing emotional content, hippocampal-amygdala dynamics facilitate consolidation over a sleep bout. This study tested if modularity and centrality-graph theoretical measures that index the level of segregation/integration in a system and the relative import of its nodes-map onto central tenets of memory consolidation theory and sleep-related processing. Findings indicate that greater network integration is tied to overnight emotional memory retention via NREM SWS expression. Greater hippocampal and amygdala influence over network organization supports emotional memory retention, and hippocampal or amygdala control over information flow are differentially associated with distinct stages of memory processing. These centrality measures are also tied to the local expression and coupling of key sleep oscillations tied to sleep-dependent memory consolidation. These findings suggest that measures of intrinsic network connectivity may predict the capacity of brain functional networks to acquire, consolidate, and retrieve emotional memories.

Keywords: consolidation; graph theory; memory; networks; resting-state; sleep.

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Preprint

Abstract

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