Verbal Learning and Memory Deficits across Neurological and Neuropsychiatric Disorders: Insights from an ENIGMA Mega Analysis

Eamonn Kennedy^{1

2

3}, Spencer W Liebel^{1

3}, Hannah M Lindsey^{1

3}, Shashank Vadlamani¹, Pui-Wa Lei⁴, Maheen M Adamson^{5

6}, Martin Alda⁷, Silvia Alonso-Lana^{8

9

10}, Tim J Anderson^{11

12

13}, Celso Arango^{9

14}, Robert F Asarnow^{15

16

17}, Mihai Avram¹⁸, Rosa Ayesa-Arriola^{9

19}, Talin Babikian^{15

20}, Nerisa Banaj²¹, Laura J Bird²², Stefan Borgwardt^{18

23}, Amy Brodtmann^{24

25}, Katharina Brosch^{26

27}, Karen Caeyenberghs²⁸, Vince D Calhoun²⁹, Nancy D Chiaravalloti^{30

31}, David X Cifu³², Benedicto Crespo-Facorro^{9

33}, John C Dalrymple-Alford^{11

12

34}, Kristen Dams-O'Connor^{35

36}, Udo Dannlowski³⁷, David Darby^{38

39

40}, Nicholas Davenport^{41

42}, John DeLuca^{31

43}, Covadonga M Diaz-Caneja¹⁴, Seth G Disner^{41

42}, Ekaterina Dobryakova^{31

44}, Stefan Ehrlich^{45

46}, Carrie Esopenko³⁵, Fabio Ferrarelli⁴⁷, Lea E Frank⁴⁸, Carol E Franz^{49

50}, Paola Fuentes-Claramonte^{8

9}, Helen Genova^{31

51}, Christopher C Giza^{20

52

53}, Janik Goltermann³⁷, Dominik Grotegerd³⁷, Marius Gruber^{37

54}, Alfonso Gutierrez-Zotes^{9

55

56}, Minji Ha⁵⁷, Jan Haavik^{58

59}, Charles Hinkin¹⁵, Kristen R Hoskinson^{60

61}, Daniela Hubl⁶², Andrei Irimia^{63

64

65}, Andreas Jansen²⁶, Michael Kaess^{66

67}, Xiaojian Kang⁵, Kimbra Kenney⁶⁸, Barbora Keřková⁶⁹, Mohamed Salah Khlif⁷⁰, Minah Kim^{71

72}, Jochen Kindler⁶⁶, Tilo Kircher²⁶, Karolina Knížková^{69

73}, Knut K Kolskår^{74

75

76}, Denise Krch^{31

44}, William S Kremen^{49

50}, Taylor Kuhn¹⁵, Veena Kumari⁷⁷, Junsoo Kwon^{57

71

72}, Roberto Langella²¹, Sarah Laskowitz⁷⁸, Jungha Lee⁵⁷, Jean Lengenfelder^{31

44}, Victoria Liou-Johnson⁵, Sara M Lippa^{79

80}, Marianne Løvstad^{75

76}, Astri J Lundervold⁸¹, Cassandra Marotta^{38

39}, Craig A Marquardt^{41

42}, Paulo Mattos⁸², Ahmad Mayeli⁴⁷, Carrie R McDonald^{83

84}, Susanne Meinert^{37

85}, Tracy R Melzer^{11

12

34}, Jessica Merchán-Naranjo¹⁴, Chantal Michel⁶⁶, Rajendra A Morey^{78

86}, Benson Mwangi⁸⁷, Daniel J Myall¹², Igor Nenadić²⁶, Mary R Newsome^{1

3}, Abraham Nunes^{7

88}, Terence O'Brien^{25

89}, Viola Oertel⁹⁰, John Ollinger⁷⁹, Alexander Olsen^{91

92

93}, Victor Ortiz García de la Foz¹⁹, Mustafa Ozmen^{2

94}, Heath Pardoe⁴⁰, Marise Parent⁹⁵, Fabrizio Piras²¹, Federica Piras²¹, Edith Pomarol-Clotet^{8

9}, Jonathan Repple^{37

54}, Geneviève Richard⁷⁴, Jonathan Rodriguez⁴⁹, Mabel Rodriguez⁶⁹, Kelly Rootes-Murdy²⁹, Jared Rowland^{96

97

98}, Nicholas P Ryan^{99

100}, Raymond Salvador^{8

9}, Anne-Marthe Sanders^{74

75

76}, Andre Schmidt¹⁰¹, Jair C Soares⁸⁷, Gianfranco Spalleta²¹, Filip Španiel^{69

102}, Scott R Sponheim^{41

42}, Alena Stasenko^{49

84}, Frederike Stein²⁶, Benjamin Straube²⁶, April Thames¹⁵, Florian Thomas-Odenthal²⁶, Sophia I Thomopoulos¹⁰³, Erin B Tone¹⁰⁴, Ivan Torres^{105

106}, Maya Troyanskaya^{107

108}, Jessica A Turner¹⁰⁹, Kristine M Ulrichsen^{74

75

76}, Guillermo Umpierrez¹¹⁰, Daniela Vecchio²¹, Elisabet Vilella^{9

55

56}, Lucy Vivash^{38

39}, William C Walker^{111

112}, Emilio Werden⁴⁰, Lars T Westlye^{74

75

113}, Krista Wild¹¹⁴, Adrian Wroblewski²⁶, Mon-Ju Wu⁸⁷, Glenn R Wylie^{31

115}, Lakshmi N Yatham¹⁰⁵, Giovana B Zunta-Soares⁸⁷, Paul M Thompson^{103

116}, Mary Jo Pugh^{1

2}, David F Tate^{1

3}, Frank G Hillary^{117

118

119}, Elisabeth A Wilde^{1

3}, Emily L Dennis^{1

3}

Affiliations

¹ Department of Neurology, University of Utah School of Medicine, Salt Lake City, UT 84132, USA.
² Division of Epidemiology, University of Utah, Salt Lake City, UT 84108, USA.
³ George E Wahlen Veterans Affairs Medical Center, Salt Lake City, UT 84148, USA.
⁴ Department of Educational Psychology, Counseling, and Special Education, Pennsylvania State University, University Park, PA 16802, USA.
⁵ WRIISC-WOMEN & Rehabilitation Department, VA Palo Alto, Palo Alto, CA 94304, USA.
⁶ Neurosurgery, Stanford School of Medicine, Stanford, CA 94305, USA.
⁷ Department of Psychiatry, Dalhousie University, Halifax, NS B3H 4R2, Canada.
⁸ FIDMAG Research Foundation, 08025 Barcelona, Spain.
⁹ Centro Investigación Biomédica en Red Salud Mental (CIBERSAM), 28029 Madrid, Spain.
¹⁰ Ace Alzheimer Center Barcelona, Universitat Internacional de Catalunya, 08022 Barcelona, Spain.
¹¹ Department of Medicine, University of Otago, Christchurch 8011, New Zealand.
¹² New Zealand Brain Research Institute, Christchurch 8011, New Zealand.
¹³ Department of Neurology, Te Whatu Ora-Health New Zealand Waitaha Canterbury, Christchurch 8011, New Zealand.
¹⁴ Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, Instituto de Investigación Sanitaria Gregorio Marañón (IiSGM), School of Medicine, Universidad Complutense, 28040 Madrid, Spain.
¹⁵ Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁶ Brain Research Institute, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁷ Department of Psychology, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁸ Translational Psychiatry, Department of Psychiatry and Psychotherapy, University of Lübeck, 23562 Lübeck, Germany.
¹⁹ Department of Psychiatry, Marqués de Valdecilla University Hospital, Instituto de Investigación Sanitaria Valdecilla (IDIVAL), School of Medicine, University of Cantabria, 39008 Santander, Spain.
²⁰ UCLA Steve Tisch BrainSPORT Program, University of California Los Angeles, Los Angeles, CA 90095, USA.
²¹ Laboratory of Neuropsychiatry, Santa Lucia Foundation IRCCS, 00179 Rome, Italy.
²² School of Clinical Sciences, Monash University, Clayton, VIC 3800, Australia.
²³ Center of Brain, Behaviour and Metabolism (CBBM), University of Lübeck, 23562 Lübeck, Germany.
²⁴ Cognitive Health Initiative, School of Translational Medicine, Monash University, Melbourne, VIC 3800, Australia.
²⁵ Department of Medicine, Royal Melbourne Hospital, Melbourne, VIC 3050, Australia.
²⁶ Department of Psychiatry and Psychotherapy, University of Marburg, 35032 Marburg, Germany.
²⁷ Institute of Behavioral Science, Feinstein Institutes for Medical Research, Manhasset, NY 11030, USA.
²⁸ Cognitive Neuroscience Unit, School of Psychology, Deakin University, Burwood, VIC 3125, Australia.
²⁹ Tri-Institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State, Georgia Tech, Emory University, Atlanta, GA 30322, USA.
³⁰ Centers for Neuropsychology, Neuroscience & Traumatic Brain Injury Research, Kessler Foundation, East Hanover, NJ 07936, USA.
³¹ Department of Physical Medicine & Rehabilitation, Rutgers, New Jersey Medical School, Newark, NJ 07103, USA.
³² Rehabilitation Medicine Department, National Institutes of Health Clinical Center, Bethesda, MD 20892, USA.
³³ Department of Psychiatry, Virgen del Rocio University Hospital, School of Medicine, University of Seville, IBIS, 41013 Seville, Spain.
³⁴ School of Psychology, Speech and Hearing, University of Canterbury, Christchurch 8041, New Zealand.
³⁵ Department of Rehabilitation and Human Performance, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁶ Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁷ Institute for Translational Psychiatry, University of Münster, 48149 Münster, Germany.
³⁸ Department of Neuroscience, Monash University, Melbourne, VIC 3800, Australia.
³⁹ Department of Neurology, Alfred Health, Melbourne, VIC 3004, Australia.
⁴⁰ The Florey Institute of Neuroscience and Mental Health, Melbourne, VIC 3052, Australia.
⁴¹ Department of Psychiatry and Behavioral Sciences, University of Minnesota Medical School, Minneapolis, MN 55455, USA.
⁴² Minneapolis VA Health Care System, Minneapolis, MN 55417, USA.
⁴³ Kessler Foundation, East Hanover, NJ 07936, USA.
⁴⁴ Center for Traumatic Brain Injury, Kessler Foundation, East Hanover, NJ 07936, USA.
⁴⁵ Translational Developmental Neuroscience Section, Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany.
⁴⁶ Eating Disorders Research and Treatment Center, Department of Child and Adolescent Psychiatry, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany.
⁴⁷ Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA.
⁴⁸ Department of Psychology, University of Oregon, Eugene, OR 97403, USA.
⁴⁹ Department of Psychiatry, University of California San Diego, La Jolla, CA 92093, USA.
⁵⁰ Center for Behavior Genetics of Aging, University of California San Diego, La Jolla, CA 92093, USA.
⁵¹ Center for Autism Research, Kessler Foundation, East Hanover, NJ 07936, USA.
⁵² Department of Pediatrics, Division of Neurology, UCLA Mattel Children's Hospital, Los Angeles, CA 90095, USA.
⁵³ Department of Neurosurgery, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA.
⁵⁴ Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Goethe University, 60590 Frankfurt, Germany.
⁵⁵ Hospital Universitari Institut Pere Mata, 43007 Tarragona, Spain.
⁵⁶ Institut d'Investiació Sanitària Pere Virgili-CERCA, Universitat Rovira i Virgili, 43007 Tarragona, Spain.
⁵⁷ Department of Brain and Cognitive Sciences, Seoul National University College of Natural Sciences, Seoul 08826, Republic of Korea.
⁵⁸ Department of Biomedicine, University of Bergen, 5007 Bergen, Norway.
⁵⁹ Division of Psychiatry, Haukeland University Hospital, 5021 Bergen, Norway.
⁶⁰ Center for Biobehavioral Health, The Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.
⁶¹ Section of Pediatrics, The Ohio State University College of Medicine, Columbus, OH 43210, USA.
⁶² Translational Research Centre, University Hospital of Psychiatry and Psychotherapy, University of Bern, 3000 Bern, Switzerland.
⁶³ Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089, USA.
⁶⁴ Department of Biomedical Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089, USA.
⁶⁵ Department of Quantitative & Computational Biology, Dornsife College of Arts & Sciences, University of Southern California, Los Angeles, CA 90089, USA.
⁶⁶ University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, 3000 Bern, Switzerland.
⁶⁷ Clinic of Child and Adolescent Psychiatry, Centre of Psychosocial Medicine, University of Heidelberg, 69120 Heidelberg, Germany.
⁶⁸ Department of Neurology, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA.
⁶⁹ National Institute of Mental Health, 250 67 Klecany, Czech Republic.
⁷⁰ Cognitive Health Initiative, Central Clinical School, Monash University, Melbourne, VIC 3800, Australia.
⁷¹ Department of Neuropsychiatry, Seoul National University Hospital, Seoul 03080, Republic of Korea.
⁷² Department of Psychiatry, Seoul National University College of Medicine, Seoul 03080, Republic of Korea.
⁷³ Department of Psychiatry, First Faculty of Medicine, Charles University and General University Hospital, 128 00 Prague, Czech Republic.
⁷⁴ Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Oslo University Hospital, 0424 Oslo, Norway.
⁷⁵ Department of Psychology, University of Oslo, 0373 Oslo, Norway.
⁷⁶ Department of Research, Sunnaas Rehabilitation Hospital, 1450 Nesodden, Norway.
⁷⁷ Department of Life Sciences, College of Health, Medicine and Life Sciences, Brunel University London, Uxbridge UB8 3PH, UK.
⁷⁸ Brain Imaging and Analysis Center, Duke University, Durham, NC 27710, USA.
⁷⁹ National Intrepid Center of Excellence, Walter Reed National Military Medical Center, Bethesda, MD 20814, USA.
⁸⁰ Department of Neuroscience, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA.
⁸¹ Department of Biological and Medical Psychology, University of Bergen, 5007 Bergen, Norway.
⁸² Institute D'Or for Research and Education (IDOR), São Paulo 04501-000, Brazil.
⁸³ Department of Radiation Medicine and Applied Sciences and Psychiatry, University of California San Diego, La Jolla, CA 92093, USA.
⁸⁴ Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA 92093, USA.
⁸⁵ Institute for Translational Neuroscience, University of Münster, 48149 Münster, Germany.
⁸⁶ VISN 6 MIRECC, Durham VA, Durham, NC 27705, USA.
⁸⁷ Center of Excellence on Mood Disorders, Louis A Faillace, MD Department of Psychiatry and Behavioral Sciences, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030, USA.
⁸⁸ Faculty of Computer Science, Dalhousie University, Halifax, NS B3H 4R2, Canada.
⁸⁹ Department of Neuroscience, The School of Translational Medicine, Alfred Health, Monash University, Melbourne VIC 3004, Australia.
⁹⁰ Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, Frankfurt University, 60590 Frankfurt, Germany.
⁹¹ Department of Psychology, Norwegian University of Science and Technology, 7491 Trondheim, Norway.
⁹² Department of Physical Medicine and Rehabilitation, St Olavs Hospital, Trondheim University Hospital, 7006 Trondheim, Norway.
⁹³ NorHEAD-Norwegian Centre for Headache Research, 7491 Trondheim, Norway.
⁹⁴ Department of Electrical and Electronics Engineering, Antalya Bilim University, 07190 Antalya, Turkey.
⁹⁵ Neuroscience Institute & Department of Psychology, Georgia State University, Atlanta, GA 30303, USA.
⁹⁶ WG (Bill) Hefner VA Medical Center, Salisbury, NC 28144, USA.
⁹⁷ Department of Neurobiology & Anatomy, Wake Forest School of Medicine, Winston-Salem, NC 27157, USA.
⁹⁸ VA Mid-Atlantic Mental Illness Research Education and Clinical Center (MA-MIRECC), Durham, NC 27705, USA.
⁹⁹ Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, VIC 3220, Australia.
¹⁰⁰ Department of Paediatrics, The University of Melbourne, Parkville, VIC 3052, Australia.
¹⁰¹ Department of Psychiatry (UPK), University of Basel, 4002 Basel, Switzerland.
¹⁰² 3rd Faculty of Medicine, Charles University, 100 00 Prague, Czech Republic.
¹⁰³ Imaging Genetics Center, Stevens Neuroimaging & Informatics Institute, Keck School of Medicine of the University of Southern California, Marina del Rey, CA 90292, USA.
¹⁰⁴ Department of Psychology, Georgia State University, Atlanta, GA 30303, USA.
¹⁰⁵ Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
¹⁰⁶ British Columbia Mental Health and Substance Use Services Research Institute, Vancouver, BC V5Z 1M9, Canada.
¹⁰⁷ Michael E DeBakey Veterans Affairs Medical Center, Houston, TX 77030, USA.
¹⁰⁸ H Ben Taub Department of Physical Medicine and Rehabilitation, Baylor College of Medicine, Houston, TX 77030, USA.
¹⁰⁹ Psychiatry and Behavioral Health, Ohio State Wexner Medical Center, Columbus, OH 43210, USA.
¹¹⁰ Division of Endocrinology, Emory University School of Medicine, Atlanta, GA 30322, USA.
¹¹¹ Department of Physical Medicine and Rehabilitation, Virginia Commonwealth University, Richmond, VA 23298, USA.
¹¹² Richmond Veterans Affairs (VA) Medical Center, Central Virginia VA Health Care System, Richmond, VA 23249, USA.
¹¹³ KG Jebsen Center for Neurodevelopmental Disorders, University of Oslo, 0372 Oslo, Norway.
¹¹⁴ Department of Psychology, Phoenix VA Health Care System, Phoenix, AZ 85012, USA.
¹¹⁵ Rocco Ortenzio Neuroimaging Center, Kessler Foundation, East Hanover, NJ 07936, USA.
¹¹⁶ Departments of Neurology, Pediatrics, Psychiatry, Radiology, Engineering, and Ophthalmology, University of Southern California, Los Angeles, CA 90089, USA.
¹¹⁷ Department of Psychology, Penn State University, State College, PA 16801, USA.
¹¹⁸ Department of Neurology, Hershey Medical Center, State College, PA 16801, USA.
¹¹⁹ Social Life and Engineering Science Imaging Center, Penn State University, State College, PA 16801, USA.

PMID: 39061410
PMCID: PMC11274572
DOI: 10.3390/brainsci14070669

Verbal Learning and Memory Deficits across Neurological and Neuropsychiatric Disorders: Insights from an ENIGMA Mega Analysis

Eamonn Kennedy et al. Brain Sci. 2024.

. 2024 Jun 29;14(7):669.

doi: 10.3390/brainsci14070669.

Authors

Affiliations

¹ Department of Neurology, University of Utah School of Medicine, Salt Lake City, UT 84132, USA.
² Division of Epidemiology, University of Utah, Salt Lake City, UT 84108, USA.
³ George E Wahlen Veterans Affairs Medical Center, Salt Lake City, UT 84148, USA.
⁴ Department of Educational Psychology, Counseling, and Special Education, Pennsylvania State University, University Park, PA 16802, USA.
⁵ WRIISC-WOMEN & Rehabilitation Department, VA Palo Alto, Palo Alto, CA 94304, USA.
⁶ Neurosurgery, Stanford School of Medicine, Stanford, CA 94305, USA.
⁷ Department of Psychiatry, Dalhousie University, Halifax, NS B3H 4R2, Canada.
⁸ FIDMAG Research Foundation, 08025 Barcelona, Spain.
⁹ Centro Investigación Biomédica en Red Salud Mental (CIBERSAM), 28029 Madrid, Spain.
¹⁰ Ace Alzheimer Center Barcelona, Universitat Internacional de Catalunya, 08022 Barcelona, Spain.
¹¹ Department of Medicine, University of Otago, Christchurch 8011, New Zealand.
¹² New Zealand Brain Research Institute, Christchurch 8011, New Zealand.
¹³ Department of Neurology, Te Whatu Ora-Health New Zealand Waitaha Canterbury, Christchurch 8011, New Zealand.
¹⁴ Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, Instituto de Investigación Sanitaria Gregorio Marañón (IiSGM), School of Medicine, Universidad Complutense, 28040 Madrid, Spain.
¹⁵ Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁶ Brain Research Institute, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁷ Department of Psychology, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁸ Translational Psychiatry, Department of Psychiatry and Psychotherapy, University of Lübeck, 23562 Lübeck, Germany.
¹⁹ Department of Psychiatry, Marqués de Valdecilla University Hospital, Instituto de Investigación Sanitaria Valdecilla (IDIVAL), School of Medicine, University of Cantabria, 39008 Santander, Spain.
²⁰ UCLA Steve Tisch BrainSPORT Program, University of California Los Angeles, Los Angeles, CA 90095, USA.
²¹ Laboratory of Neuropsychiatry, Santa Lucia Foundation IRCCS, 00179 Rome, Italy.
²² School of Clinical Sciences, Monash University, Clayton, VIC 3800, Australia.
²³ Center of Brain, Behaviour and Metabolism (CBBM), University of Lübeck, 23562 Lübeck, Germany.
²⁴ Cognitive Health Initiative, School of Translational Medicine, Monash University, Melbourne, VIC 3800, Australia.
²⁵ Department of Medicine, Royal Melbourne Hospital, Melbourne, VIC 3050, Australia.
²⁶ Department of Psychiatry and Psychotherapy, University of Marburg, 35032 Marburg, Germany.
²⁷ Institute of Behavioral Science, Feinstein Institutes for Medical Research, Manhasset, NY 11030, USA.
²⁸ Cognitive Neuroscience Unit, School of Psychology, Deakin University, Burwood, VIC 3125, Australia.
²⁹ Tri-Institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State, Georgia Tech, Emory University, Atlanta, GA 30322, USA.
³⁰ Centers for Neuropsychology, Neuroscience & Traumatic Brain Injury Research, Kessler Foundation, East Hanover, NJ 07936, USA.
³¹ Department of Physical Medicine & Rehabilitation, Rutgers, New Jersey Medical School, Newark, NJ 07103, USA.
³² Rehabilitation Medicine Department, National Institutes of Health Clinical Center, Bethesda, MD 20892, USA.
³³ Department of Psychiatry, Virgen del Rocio University Hospital, School of Medicine, University of Seville, IBIS, 41013 Seville, Spain.
³⁴ School of Psychology, Speech and Hearing, University of Canterbury, Christchurch 8041, New Zealand.
³⁵ Department of Rehabilitation and Human Performance, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁶ Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁷ Institute for Translational Psychiatry, University of Münster, 48149 Münster, Germany.
³⁸ Department of Neuroscience, Monash University, Melbourne, VIC 3800, Australia.
³⁹ Department of Neurology, Alfred Health, Melbourne, VIC 3004, Australia.
⁴⁰ The Florey Institute of Neuroscience and Mental Health, Melbourne, VIC 3052, Australia.
⁴¹ Department of Psychiatry and Behavioral Sciences, University of Minnesota Medical School, Minneapolis, MN 55455, USA.
⁴² Minneapolis VA Health Care System, Minneapolis, MN 55417, USA.
⁴³ Kessler Foundation, East Hanover, NJ 07936, USA.
⁴⁴ Center for Traumatic Brain Injury, Kessler Foundation, East Hanover, NJ 07936, USA.
⁴⁵ Translational Developmental Neuroscience Section, Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany.
⁴⁶ Eating Disorders Research and Treatment Center, Department of Child and Adolescent Psychiatry, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany.
⁴⁷ Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA.
⁴⁸ Department of Psychology, University of Oregon, Eugene, OR 97403, USA.
⁴⁹ Department of Psychiatry, University of California San Diego, La Jolla, CA 92093, USA.
⁵⁰ Center for Behavior Genetics of Aging, University of California San Diego, La Jolla, CA 92093, USA.
⁵¹ Center for Autism Research, Kessler Foundation, East Hanover, NJ 07936, USA.
⁵² Department of Pediatrics, Division of Neurology, UCLA Mattel Children's Hospital, Los Angeles, CA 90095, USA.
⁵³ Department of Neurosurgery, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA.
⁵⁴ Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Goethe University, 60590 Frankfurt, Germany.
⁵⁵ Hospital Universitari Institut Pere Mata, 43007 Tarragona, Spain.
⁵⁶ Institut d'Investiació Sanitària Pere Virgili-CERCA, Universitat Rovira i Virgili, 43007 Tarragona, Spain.
⁵⁷ Department of Brain and Cognitive Sciences, Seoul National University College of Natural Sciences, Seoul 08826, Republic of Korea.
⁵⁸ Department of Biomedicine, University of Bergen, 5007 Bergen, Norway.
⁵⁹ Division of Psychiatry, Haukeland University Hospital, 5021 Bergen, Norway.
⁶⁰ Center for Biobehavioral Health, The Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.
⁶¹ Section of Pediatrics, The Ohio State University College of Medicine, Columbus, OH 43210, USA.
⁶² Translational Research Centre, University Hospital of Psychiatry and Psychotherapy, University of Bern, 3000 Bern, Switzerland.
⁶³ Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089, USA.
⁶⁴ Department of Biomedical Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089, USA.
⁶⁵ Department of Quantitative & Computational Biology, Dornsife College of Arts & Sciences, University of Southern California, Los Angeles, CA 90089, USA.
⁶⁶ University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, 3000 Bern, Switzerland.
⁶⁷ Clinic of Child and Adolescent Psychiatry, Centre of Psychosocial Medicine, University of Heidelberg, 69120 Heidelberg, Germany.
⁶⁸ Department of Neurology, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA.
⁶⁹ National Institute of Mental Health, 250 67 Klecany, Czech Republic.
⁷⁰ Cognitive Health Initiative, Central Clinical School, Monash University, Melbourne, VIC 3800, Australia.
⁷¹ Department of Neuropsychiatry, Seoul National University Hospital, Seoul 03080, Republic of Korea.
⁷² Department of Psychiatry, Seoul National University College of Medicine, Seoul 03080, Republic of Korea.
⁷³ Department of Psychiatry, First Faculty of Medicine, Charles University and General University Hospital, 128 00 Prague, Czech Republic.
⁷⁴ Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Oslo University Hospital, 0424 Oslo, Norway.
⁷⁵ Department of Psychology, University of Oslo, 0373 Oslo, Norway.
⁷⁶ Department of Research, Sunnaas Rehabilitation Hospital, 1450 Nesodden, Norway.
⁷⁷ Department of Life Sciences, College of Health, Medicine and Life Sciences, Brunel University London, Uxbridge UB8 3PH, UK.
⁷⁸ Brain Imaging and Analysis Center, Duke University, Durham, NC 27710, USA.
⁷⁹ National Intrepid Center of Excellence, Walter Reed National Military Medical Center, Bethesda, MD 20814, USA.
⁸⁰ Department of Neuroscience, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA.
⁸¹ Department of Biological and Medical Psychology, University of Bergen, 5007 Bergen, Norway.
⁸² Institute D'Or for Research and Education (IDOR), São Paulo 04501-000, Brazil.
⁸³ Department of Radiation Medicine and Applied Sciences and Psychiatry, University of California San Diego, La Jolla, CA 92093, USA.
⁸⁴ Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA 92093, USA.
⁸⁵ Institute for Translational Neuroscience, University of Münster, 48149 Münster, Germany.
⁸⁶ VISN 6 MIRECC, Durham VA, Durham, NC 27705, USA.
⁸⁷ Center of Excellence on Mood Disorders, Louis A Faillace, MD Department of Psychiatry and Behavioral Sciences, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030, USA.
⁸⁸ Faculty of Computer Science, Dalhousie University, Halifax, NS B3H 4R2, Canada.
⁸⁹ Department of Neuroscience, The School of Translational Medicine, Alfred Health, Monash University, Melbourne VIC 3004, Australia.
⁹⁰ Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, Frankfurt University, 60590 Frankfurt, Germany.
⁹¹ Department of Psychology, Norwegian University of Science and Technology, 7491 Trondheim, Norway.
⁹² Department of Physical Medicine and Rehabilitation, St Olavs Hospital, Trondheim University Hospital, 7006 Trondheim, Norway.
⁹³ NorHEAD-Norwegian Centre for Headache Research, 7491 Trondheim, Norway.
⁹⁴ Department of Electrical and Electronics Engineering, Antalya Bilim University, 07190 Antalya, Turkey.
⁹⁵ Neuroscience Institute & Department of Psychology, Georgia State University, Atlanta, GA 30303, USA.
⁹⁶ WG (Bill) Hefner VA Medical Center, Salisbury, NC 28144, USA.
⁹⁷ Department of Neurobiology & Anatomy, Wake Forest School of Medicine, Winston-Salem, NC 27157, USA.
⁹⁸ VA Mid-Atlantic Mental Illness Research Education and Clinical Center (MA-MIRECC), Durham, NC 27705, USA.
⁹⁹ Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, VIC 3220, Australia.
¹⁰⁰ Department of Paediatrics, The University of Melbourne, Parkville, VIC 3052, Australia.
¹⁰¹ Department of Psychiatry (UPK), University of Basel, 4002 Basel, Switzerland.
¹⁰² 3rd Faculty of Medicine, Charles University, 100 00 Prague, Czech Republic.
¹⁰³ Imaging Genetics Center, Stevens Neuroimaging & Informatics Institute, Keck School of Medicine of the University of Southern California, Marina del Rey, CA 90292, USA.
¹⁰⁴ Department of Psychology, Georgia State University, Atlanta, GA 30303, USA.
¹⁰⁵ Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
¹⁰⁶ British Columbia Mental Health and Substance Use Services Research Institute, Vancouver, BC V5Z 1M9, Canada.
¹⁰⁷ Michael E DeBakey Veterans Affairs Medical Center, Houston, TX 77030, USA.
¹⁰⁸ H Ben Taub Department of Physical Medicine and Rehabilitation, Baylor College of Medicine, Houston, TX 77030, USA.
¹⁰⁹ Psychiatry and Behavioral Health, Ohio State Wexner Medical Center, Columbus, OH 43210, USA.
¹¹⁰ Division of Endocrinology, Emory University School of Medicine, Atlanta, GA 30322, USA.
¹¹¹ Department of Physical Medicine and Rehabilitation, Virginia Commonwealth University, Richmond, VA 23298, USA.
¹¹² Richmond Veterans Affairs (VA) Medical Center, Central Virginia VA Health Care System, Richmond, VA 23249, USA.
¹¹³ KG Jebsen Center for Neurodevelopmental Disorders, University of Oslo, 0372 Oslo, Norway.
¹¹⁴ Department of Psychology, Phoenix VA Health Care System, Phoenix, AZ 85012, USA.
¹¹⁵ Rocco Ortenzio Neuroimaging Center, Kessler Foundation, East Hanover, NJ 07936, USA.
¹¹⁶ Departments of Neurology, Pediatrics, Psychiatry, Radiology, Engineering, and Ophthalmology, University of Southern California, Los Angeles, CA 90089, USA.
¹¹⁷ Department of Psychology, Penn State University, State College, PA 16801, USA.
¹¹⁸ Department of Neurology, Hershey Medical Center, State College, PA 16801, USA.
¹¹⁹ Social Life and Engineering Science Imaging Center, Penn State University, State College, PA 16801, USA.

PMID: 39061410
PMCID: PMC11274572
DOI: 10.3390/brainsci14070669

Abstract

Deficits in memory performance have been linked to a wide range of neurological and neuropsychiatric conditions. While many studies have assessed the memory impacts of individual conditions, this study considers a broader perspective by evaluating how memory recall is differentially associated with nine common neuropsychiatric conditions using data drawn from 55 international studies, aggregating 15,883 unique participants aged 15-90. The effects of dementia, mild cognitive impairment, Parkinson's disease, traumatic brain injury, stroke, depression, attention-deficit/hyperactivity disorder (ADHD), schizophrenia, and bipolar disorder on immediate, short-, and long-delay verbal learning and memory (VLM) scores were estimated relative to matched healthy individuals. Random forest models identified age, years of education, and site as important VLM covariates. A Bayesian harmonization approach was used to isolate and remove site effects. Regression estimated the adjusted association of each clinical group with VLM scores. Memory deficits were strongly associated with dementia and schizophrenia (p < 0.001), while neither depression nor ADHD showed consistent associations with VLM scores (p > 0.05). Differences associated with clinical conditions were larger for longer delayed recall duration items. By comparing VLM across clinical conditions, this study provides a foundation for enhanced diagnostic precision and offers new insights into disease management of comorbid disorders.

Keywords: Parkinson’s disease; attention-deficit/hyperactivity disorder; bipolar disorder; dementia; depression; memory; schizophrenia; stroke; traumatic brain injury; verbal learning.

PubMed Disclaimer

Conflict of interest statement

Celso Arango has been a consultant to or has received honoraria or grants from Abbot, Acadia, Ambrosetti, Angelini, Biogen, Boehringer, Gedeon Richter, Janssen Cilag, Lundbeck, Medscape, Menarini, Minerva, Otsuka, Pfizer, Roche, Sage, Servier, Shire, Schering Plough, Sumitomo Dainippon Pharma, Sunovion, Takeda, and Teva. Amy Brodtmann serves on the editorial boards of Neurology and International Journal of Stroke. Benedicto Crespo-Facorro has been a consultant to or has received honoraria or grants from Angelini, Boehringer, Johnson, Lundbeck, Otsuka, and Rovi. Covadonga M. Diaz-Caneja has received honoraria from Angelini and Viatris. Christopher C. Giza has been a consultant to the NBA, NFL, NHLPA, and Los Angeles Lakers, he has served on the advisory board for Highmark Interactive, Novartis, MLS, NBA, and USSF, and he handles 1–2 medicolegal cases annually. Jonathan Repple has received speaking honoraria from Janssen and Hexal. Jair C. Soares has been a consultant to, has received honoraria or grants from, or has stock in Alkermes, Allergan, Asofarma, ATAI, Boehringer Ingelheim, Compass, Johnson & Johnson, Livanova, Pfizer, Pulvinar Neuro LLC, Relmada, Sanofi, and Sunovian. Paul M. Thompson received partial research support from Biogen, Inc., for research unrelated to this manuscript. Lucy Vivash received partial research support for this project by an investigator-initiated research grant from Biogen (US). Biogen had no role in the analysis or writing of this manuscript. Additionally, Lucy Vivash received support from Eisai (JP) and Life Molecular Imaging for research unrelated to this manuscript. Glenn R. Wylie has received research support from the NJ Commission for Brain Injury Research, the Dept of Veterans Affairs, Biogen, Bristol, Myers, Squibb, and Genetech, and he has served on advisory boards for the CDMRP and the VA; all of these activities are unrelated to this research. Lakshmi N. Yatham has been on speaker or advisory boards for, or has received research grants from, Alkermes, Abbvie, Canadian Institutes of Health Research, Sumitomo Dainippon Pharma, GlaxoSmithKline, Intracellular Therapies, Merck, Sanofi, Sequiris, Servier, and Sunovion, all outside this work. David F. Tate received funding from the Defense and Veterans Brain Injury Centers, the U.S. Army Medical Research and Materiel Command, and the Chronic Effects of Neurotrauma Consortium (CENC). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results. All other authors declare no conflicts of interest. The views expressed in this article are those of the author(s) and do not reflect the official policy of the Department of Army/Navy/Air Force, Department of Defense, or U.S. Government.

Figures

**Figure 1**
World map showing the locations of participating collaborator institutions (triangles). Details for each sub-study are provided in Supplementary Table S1.

**Figure 2**
Preliminary screening of covariates by random forest models. In (a), feature importances identified age, education, and site as the most important variables for adjustment. In (b), raw Trials 1–5 scores are plotted against Trials 1–5 scores after source correction (color indicates origin study). Gray lines show the fits used to correct for each site.

**Figure 3**
Percentage changes in words recalled are shown for each clinical group relative to matched controls. Numerical data for this figure are available in Supplementary Table S2. MDD = major depressive disorder. ADHD = attention-deficit/hyperactivity disorder. TBI = traumatic brain injury. BD = bipolar disorder. PD = Parkinson’s disease. SZ = schizophrenia. MCI = mild cognitive impairment. AD/RD = Alzheimer’s disease and related dementias. T1 = immediate recall trial 1. Trials 1–5 = total score across immediate recall/learning trials 1–5. SDFR = short-delay free recall. LDFR = long-delay free recall. * significant at p < 0.01 for all four items.

**Figure 4**
Age- (a) and sex/gender- (b) stratified percentage score differences across female/male and above/below median age groups relative to matched controls. MDD = major depressive disorder. ADHD = attention-deficit/hyperactivity disorder. TBI = traumatic brain injury. BD = bipolar disorder. PD = Parkinson’s disease. SZ = schizophrenia. MCI = mild cognitive impairment. AD/RD = Alzheimer’s disease and related dementias. T1 = immediate recall trial 1. Trials 1–5 = total score across immediate recall/learning trials 1–5. SDFR = short-delay free recall. LDFR = long-delay free recall.

See this image and copyright information in PMC

References

1. Katz J., Saadon-Grosman N., Arzy S. The life review experience: Qualitative and quantitative characteristics. Conscious. Cogn. 2017;48:76–86. doi: 10.1016/j.concog.2016.10.011. - DOI - PubMed
1. Maki Y., Yamaguchi T., Yamagami T., Murai T., Hachisuka K., Miyamae F., Ito K., Awata S., Ura C., Takahashi R., et al. The impact of subjective memory complaints on quality of life in community-dwelling older adults. Psychogeriatrics. 2014;14:175–181. doi: 10.1111/psyg.12056. - DOI - PubMed
1. Arvanitakis Z., Shah R.C., Bennett D.A. Diagnosis and Management of Dementia: Review. JAMA. 2019;322:1589–1599. doi: 10.1001/jama.2019.4782. - DOI - PMC - PubMed
1. Jongsiriyanyong S., Limpawattana P. Mild Cognitive Impairment in Clinical Practice: A Review Article. Am. J. Alzheimers Dis. Other Demen. 2018;33:500–507. doi: 10.1177/1533317518791401. - DOI - PMC - PubMed
1. Faglioni P., Saetti M.C., Botti C. Verbal learning strategies in Parkinson’s disease. Neuropsychology. 2000;14:456–470. doi: 10.1037/0894-4105.14.3.456. - DOI - PubMed

Grants and funding

LinkOut - more resources

Full Text Sources
Miscellaneous
- NCI CPTAC Assay Portal

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Verbal Learning and Memory Deficits across Neurological and Neuropsychiatric Disorders: Insights from an ENIGMA Mega Analysis

Affiliations

Verbal Learning and Memory Deficits across Neurological and Neuropsychiatric Disorders: Insights from an ENIGMA Mega Analysis

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Grants and funding

LinkOut - more resources

Full Text Sources

Miscellaneous