Resting-State Hyperperfusion of the Supplementary Motor Area in Catatonia

Abstract

Catatonia is a psychomotor syndrome that not only frequently occurs in the context of schizophrenia but also in other conditions. The neural correlates of catatonia remain unclear due to small-sized studies. We therefore compared resting-state cerebral blood flow (rCBF) and gray matter (GM) density between schizophrenia patients with current catatonia and without catatonia and healthy controls. We included 42 schizophrenia patients and 41 controls. Catatonia was currently present in 15 patients (scoring >2 items on the Bush Francis Catatonia Rating Scale screening). Patients did not differ in antipsychotic medication or positive symptoms. We acquired whole-brain rCBF using arterial spin labeling and GM density. We compared whole-brain perfusion and GM density over all and between the groups using 1-way ANCOVAs (F and T tests). We found a group effect (F test) of rCBF within bilateral supplementary motor area (SMA), anterior cingulate cortex, dorsolateral prefrontal cortex, left interior parietal lobe, and cerebellum. T tests indicated 1 cluster (SMA) to be specific to catatonia. Moreover, catatonia of excited and retarded types differed in SMA perfusion. Furthermore, increased catatonia severity was associated with higher perfusion in SMA. Finally, catatonia patients had a distinct pattern of GM density reduction compared to controls with prominent GM loss in frontal and insular cortices. SMA resting-state hyperperfusion is a marker of current catatonia in schizophrenia. This is highly compatible with a dysregulated motor system in catatonia, particularly affecting premotor areas. Moreover, SMA perfusion was differentially altered in retarded and excited catatonia subtypes, arguing for distinct pathobiology.

Aberrant Middle Prefrontal-Motor Cortex Connectivity Mediates Motor Inhibitory Biomarker in Schizophrenia

“…For example, catatonic patients not only exhibited prefrontal hypoactivation and frontal gray matter loss(17,59), but also had altered connections between PFC and premotor/motor cortex(60). In a recent study of Walther and colleagues, catatonia was associated with higher perfusion in supplementary motor area and prominent GM loss in frontal and insular cortices(61), which resemble the SICI-related PFC and insula clusters observed in our study. Schizophrenia patients with severe gesture deficits showed poor frontal lobe function(62,63).…”

“…This is consistent with the literature. The cerebellar-motor circuit is linked to deficit of sensorimotor control in schizophrenia(17,61,82) and stimulation of cerebellum altered the size of SICI at motor cortex(83); and the involvement of cerebellum in the neuropathology of schizophrenia is well supported(82,84). However, it should be noted that the association between SICI and cerebellum did not pass LOOCV test and this finding need to be confirmed by future studies.…”

Systems Neuroscience of Psychosis: Mapping Schizophrenia Symptoms onto Brain Systems

“…In particular, we demonstrated resting-state hyperperfusion in the supplementary motor area (SMA) of subjects with current catatonia in schizophrenia [124]. This finding was specific to subjects suffering from current catatonia in the context of schizophrenia.…”

“…In particular, a recent study on akinetic catatonia offered a direct hint on a clinical application. Regional SMA hyperactivity was found to be a possible cause of the severe behavioral inhibition, indicating that this cortical regional is a possible target for inhibitory rTMS [124]. …”

Motor system dysfunction in the schizophrenia diathesis: Neural systems to neurotransmitters

“…For example, volumetric reductions and fMRI measures of activation are negatively correlated with NSS scores in the SMA and M1 of recently diagnosed patients (92-94). Alterations in the size of the SMA are also thought to represent a compensatory cortico-cortical pathway that may offset insufficient basal ganglia output (95), and in catatonic patients with schizophrenia, increased severity of catatonia (based on the Bush Francis Catatonia Rating scale) predicts higher blood perfusion in the SMA (96). This latter effect is highly suggestive that schizophrenia is associated with dysregulation of the SMA in the resting state.…”