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 control individuals (NCs). Most previous studies examined the thalamus as a whole as a single region of interest. In addition, findings in individuals at familial high risk for SCZ (FHRs) remain inconclusive. Here, we investigated whether local and network-wide thalamic-related structural alterations vary as a function of familial risk for SCZ. Methods: Structural magnetic resonance imaging scans were obtained from 5197 participants (NC, n = 3409; FHR, n = 257; SCZ, n = 1531) across 32 cross-sectional samples within the ENIGMA (Enhancing Neuro Imaging Genetics through Meta Analysis) Consortium. Random-effects meta-analyses and network analyses were conducted on 1) local thalamic alterations (volume estimates of 7 thalamic subdivisions) and 2) network-wide thalamic alterations (thickness and surface-related thalamocortical/corticocortical covariation 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 with NCs (false discovery rate–corrected q [q FDR] < .05). FHRs did not differ from NCs. At the network-wide level, thalamocortical covariations discriminated FHRs from NCs (q FDR < .05), with FHRs showing intermediate covariation between individuals with SCZ and NCs. Corticocortical covariation patterns revealed that individuals with SCZ and FHRs shared similarly disconnected clustering configurations, distinct from NCs (q FDR < .05). Conclusions: Results revealed lower thalamic volume estimates in individuals with SCZ but not in FHRs, hence yielding no evidence of a familial risk trait, whereas thalamocortical and corticocortical covariation estimates were associated with familial risk for SCZ. These findings suggest that, once the thalamus is parsed into subdivisions, network-wide thalamocortical features may identify trait-dependent, neurobiological correlates of genetic risk for SCZ.

Original languageEnglish
Pages (from-to)698-711
Number of pages14
JournalBiological Psychiatry
Volume98
Issue number9
Early online date7 May 2025
DOIs
Publication statusPublished - 1 Nov 2025

Keywords

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

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