Increased cortical thickness in nodes of the cognitive control and default mode networks in psychosis of epilepsy

James Allebone; Sarah J Wilson; Richard C J Bradlow; Jerome Maller; Terry O'Brien; Saul A Mullen; Mark Cook; Sophia J Adams; Simon Vogrin; David N Vaughan; Alan Connelly; Patrick Kwan; Samuel F Berkovic; Wendyl J D'Souza; Graeme Jackson; Dennis Velakoulis; Richard A Kanaan

doi:10.1016/j.seizure.2022.09.006

Increased cortical thickness in nodes of the cognitive control and default mode networks in psychosis of epilepsy

Seizure. 2022 Oct:101:244-252. doi: 10.1016/j.seizure.2022.09.006. Epub 2022 Sep 8.

Authors

James Allebone¹, Sarah J Wilson², Richard C J Bradlow³, Jerome Maller⁴, Terry O'Brien⁵, Saul A Mullen⁶, Mark Cook⁷, Sophia J Adams⁸, Simon Vogrin⁹, David N Vaughan¹⁰, Alan Connelly¹⁰, Patrick Kwan⁵, Samuel F Berkovic¹¹, Wendyl J D'Souza¹², Graeme Jackson¹⁰, Dennis Velakoulis¹³, Richard A Kanaan¹⁴

Affiliations

¹ Melbourne School of Psychological Sciences, University of Melbourne, VIC, Australia; The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria, Australia.
² Melbourne School of Psychological Sciences, University of Melbourne, VIC, Australia; The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria, Australia; Comprehensive Epilepsy Program, Austin Health, University of Melbourne, Victoria, Australia.
³ Turning Point, Eastern Health, Victoria, Australia.
⁴ ANU College of Health and Medicine, Australian National University, Canberra, Victoria, Australia; Monash Alfred Psychiatry Research Centre, The Alfred and Monash University, Melbourne, Australia.
⁵ Royal Melbourne Hospital, Melbourne, Victoria, Australia; Department of Neuroscience, Alfred Hospital, Monash University, Melbourne, Australia.
⁶ The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria, Australia.
⁷ Graeme Clark Institute, University of Melbourne, Melbourne, Australia.
⁸ Department of Psychiatry, Austin Health, University of Melbourne, Melbourne, Australia.
⁹ St Vincent's Hospital, Melbourne, Victoria, Australia.
¹⁰ The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria, Australia; Comprehensive Epilepsy Program, Austin Health, University of Melbourne, Victoria, Australia.
¹¹ Comprehensive Epilepsy Program, Austin Health, University of Melbourne, Victoria, Australia.
¹² Department of Medicine, St Vincent's Hospital, The University of Melbourne, Australia.
¹³ Neuropsychiatry Unit, Royal Melbourne Hospital, Melbourne, Victoria, Australia; Melbourne Neuropsychiatry Centre, University of Melbourne and Melbourne Health, Melbourne, Australia.
¹⁴ The Florey Institute of Neuroscience and Mental Health, Parkville, Victoria, Australia; Department of Psychiatry, Austin Health, University of Melbourne, Melbourne, Australia. Electronic address: richard.kanaan@unimelb.edu.au.

PMID: 36116283
DOI: 10.1016/j.seizure.2022.09.006

Abstract

Objective: To explore the cortical morphological associations of the psychoses of epilepsy.

Methods: Psychosis of epilepsy (POE) has two main subtypes - postictal psychosis and interictal psychosis. We used automated surface-based analysis of magnetic resonance images to compare cortical thickness, area, and volume across the whole brain between: (i) all patients with POE (n = 23) relative to epilepsy-without psychosis controls (EC; n = 23), (ii) patients with interictal psychosis (n = 10) or postictal psychosis (n = 13) relative to EC, and (iii) patients with postictal psychosis (n = 13) relative to patients with interictal psychosis (n = 10).

Results: POE is characterised by cortical thickening relative to EC, occurring primarily in nodes of the cognitive control network; (rostral anterior cingulate, caudal anterior cingulate, middle frontal gyrus), and the default mode network (posterior cingulate, medial paracentral gyrus, and precuneus). Patients with interictal psychosis displayed cortical thickening in the left hemisphere in occipital and temporal regions relative to EC (lateral occipital cortex, lingual, fusiform, and inferior temporal gyri), which was evident to a lesser extent in postictal psychosis patients. There were no significant differences in cortical thickness, area, or volume between the postictal psychosis and EC groups, or between the postictal psychosis and interictal psychosis groups. However, prior to correction for multiple comparisons, both the interictal psychosis and postictal psychosis groups displayed cortical thickening relative to EC in highly similar regions to those identified in the POE group overall.

Significance: The results show cortical thickening in POE overall, primarily in nodes of the cognitive control and default mode networks, compared to patients with epilepsy without psychosis. Additional thickening in temporal and occipital neocortex implicated in the dorsal and ventral visual pathways may differentiate interictal psychosis from postictal psychosis. A novel mechanism for cortical thickening in POE is proposed whereby normal synaptic pruning processes are interrupted by seizure onset.

Keywords: Cortex; Epilepsy; Interictal psychosis; Postictal psychosis; Psychosis.

MeSH terms

Cognition
Electroencephalography / methods
Epilepsy* / psychology
Humans
Magnetic Resonance Imaging / methods
Psychotic Disorders* / diagnostic imaging
Seizures