Thalamo-cortical structural co-variation networks are related to familial risk for schizophrenia in the context of lower nuclei volume estimates in patients: an ENIGMA study

Annalisa Lella, Linda A Antonucci, Roberta Passiatore, Loredana Bellantuono, Pierluigi Selvaggi, Teresa Popolizio, Guido Di Sciascio, Alessandro Saponaro, Patrizia Ricci, Mario Altamura, Giuseppe Blasi, Antonio Rampino, Chris Vriend, Vince D Calhoun, Kelly Rootes-Murdy, Aaron L Goldman, Inmaculada Baeza, Josefina Castro-Fornieles, Gisela Sugranyes, Elena De la SernaEdith Pomarol-Clotet, Mar Fatjó-Vilas, Raymond Salvador, Andriana Karuk, Paola Fuentes-Claramonte, David C Glahn, Amanda L Rodrigue, John Blangero, Lei Wang, Taeyoung Lee, Karolin E Einenkel, Saskia Hamers, Oliver Gruber, Adrian Preda, Young-Chul Chung, Soyolsaikhan Odkhuu, Corentin Vallée, Paola Dazzan, Machteld Marcelis, Stijn Michielse, Katharina Brosch, Frederike Stein, Igor Nenadic, Benjamin Straube, Florian Thomas-Odenthal, Tilo Kircher, Sean Carruthers, Susan L Rossell, Phillip J Sumner, Tamsyn E Van Rheenen, Apulian Network on Risk for Psychosis

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

BACKGROUND: Structural brain differences in the thalamus and the cortex have been widely reported in schizophrenia (SCZ) relative to neurotypical controls (NC). Most prior studies examined the thalamus as a whole, single region-of-interest. Additionally, findings in individuals at familial high-risk for schizophrenia (FHR) remain inconclusive. Here, we investigated whether local and network-wide thalamic-related structural alterations vary as a function of familial risk for schizophrenia. METHODS: Structural MRI scans were obtained from 5,197 participants (3,409 NC, 257 FHR, 1,531 SCZ) across 32 cross-sectional samples within the ENIGMA Consortium. Random-effects meta-analyses, and network analyses were conducted on (i) local thalamic alterations (volume estimates of seven thalamic subdivisions), and (ii) network-wide thalamic alterations (thickness and surface-related thalamo-cortical/cortico-cortical co-variation patterns) across groups (NC, FHR, SCZ). RESULTS: Individuals with SCZ showed significantly lower gray matter volume estimates in the anterior, pulvinar, medial, posterior, and ventral thalamic subdivisions compared to NC (q <0.05). FHR did not differ from NC. At the network-wide level, thalamo-cortical co-variations discriminated FHR from NC (q <0.05), with FHR showing intermediate co-variation between SCZ and NC. Cortico-cortical co-variation patterns revealed that SCZ and FHR shared similarly disconnected clustering configurations, distinct from NC (q <0.05). CONCLUSIONS: Results revealed lower thalamic volume estimates in SCZ but not in FHR, hence yielding no evidence of a familial risk trait, whereas thalamo-cortical and cortico-cortical co-variation estimates were associated with familial risk for SCZ These findings suggest that, once the thalamus is parsed into subdivisions, network-wide thalamo-cortical features may identify trait-dependent, neurobiological correlates of genetic risk for SCZ.
Original languageEnglish
JournalBiological Psychiatry
DOIs
Publication statusE-pub ahead of print - 7 May 2025

Keywords

  • Familial high risk for schizophrenia
  • meta-analyses
  • morphometric measures
  • structural neuroimaging
  • thalamic subdivisions
  • thalamo-cortical networks

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