Cortical and white matter substrates supporting visuospatial working memory

Riyo Ueda; Kazuki Sakakura; Takumi Mitsuhashi; Masaki Sonoda; Ethan Firestone; Naoto Kuroda; Yu Kitazawa; Hiroshi Uda; Aimee F Luat; Elizabeth L Johnson; Noa Ofen; Eishi Asano

doi:10.1016/j.clinph.2024.03.008

Cortical and white matter substrates supporting visuospatial working memory

Clin Neurophysiol. 2024 Mar 18:162:9-27. doi: 10.1016/j.clinph.2024.03.008. Online ahead of print.

Authors

Riyo Ueda¹, Kazuki Sakakura², Takumi Mitsuhashi³, Masaki Sonoda⁴, Ethan Firestone⁵, Naoto Kuroda⁶, Yu Kitazawa⁷, Hiroshi Uda⁸, Aimee F Luat⁹, Elizabeth L Johnson¹⁰, Noa Ofen¹¹, Eishi Asano¹²

Affiliations

¹ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; National Center Hospital, National Center of Neurology and Psychiatry, Tokyo 1878551, Japan. Electronic address: hj9794@wayne.edu.
² Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurosurgery, Rush University Medical Center, Chicago, Illinois 60612, USA; Department of Neurosurgery, University of Tsukuba, Tsukuba 3058575, Japan. Electronic address: Kazuki_Sakakura@rush.edu.
³ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurosurgery, Juntendo University, School of Medicine, Tokyo 1138421, Japan. Electronic address: tmituha@juntendo.ac.jp.
⁴ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurosurgery, Yokohama City University, Yokohama 2360004, Japan. Electronic address: sonoda.mas.pu@yokohama-cu.ac.jp.
⁵ Department of Physiology, Wayne State University, Detroit, Michigan 48202, USA. Electronic address: efirest@med.wayne.edu.
⁶ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Epileptology, Tohoku University Graduate School of Medicine, Sendai 9808575, Japan. Electronic address: naoto.kuroda@wayne.edu.
⁷ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurology and Stroke Medicine, Yokohama City University, Yokohama 2360004, Japan. Electronic address: yu_kitazawa@wayne.edu.
⁸ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurosurgery, Osaka Metropolitan University Graduate School of Medicine, Osaka 5458585, Japan. Electronic address: hm9480@wayne.edu.
⁹ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurology, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Pediatrics, Central Michigan University, Mt. Pleasant, Michigan 48858, USA. Electronic address: aluat@dmc.org.
¹⁰ Departments of Medical Social Sciences, Pediatrics, and Psychology, Northwestern University, Chicago, Illinois 60611, USA. Electronic address: eljohnson@northwestern.edu.
¹¹ Life-Span Cognitive Neuroscience Program, Institute of Gerontology and Merrill Palmer Skillman Institute, Wayne State University, Detroit, Michigan 48202, USA; Department of Psychology, Wayne State University, Detroit, Michigan 48202, USA. Electronic address: noa.ofen@wayne.edu.
¹² Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurology, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, Michigan 48201, USA; Translational Neuroscience Program, Wayne State University, Detroit, Michigan 48201, USA. Electronic address: easano@med.wayne.edu.

PMID: 38552414
DOI: 10.1016/j.clinph.2024.03.008

Abstract

Objective: In tasks involving new visuospatial information, we rely on working memory, supported by a distributed brain network. We investigated the dynamic interplay between brain regions, including cortical and white matter structures, to understand how neural interactions change with different memory loads and trials, and their subsequent impact on working memory performance.

Methods: Patients undertook a task of immediate spatial recall during intracranial EEG monitoring. We charted the dynamics of cortical high-gamma activity and associated functional connectivity modulations in white matter tracts.

Results: Elevated memory loads were linked to enhanced functional connectivity via occipital longitudinal tracts, yet decreased through arcuate, uncinate, and superior-longitudinal fasciculi. As task familiarity grew, there was increased high-gamma activity in the posterior inferior-frontal gyrus (pIFG) and diminished functional connectivity across a network encompassing frontal, parietal, and temporal lobes. Early pIFG high-gamma activity was predictive of successful recall. Including this metric in a logistic regression model yielded an accuracy of 0.76.

Conclusions: Optimizing visuospatial working memory through practice is tied to early pIFG activation and decreased dependence on irrelevant neural pathways.

Significance: This study expands our knowledge of human adaptation for visuospatial working memory, showing the spatiotemporal dynamics of cortical network modulations through white matter tracts.

Keywords: Broadband high-frequency activity; Functional brain mapping; Intracranial EEG recording; Pediatric epilepsy surgery; Physiological high-frequency oscillations (HFOs).