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Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain

Nicholas D. Schiff, Urs Ribary, Diana Rodriguez Moreno, Bradley Beattie, Eugene Kronberg, Ronald Blasberg, Joseph Giacino, Caroline McCagg, Joseph J. Fins, Rodolfo Llinás, Fred Plum
DOI: http://dx.doi.org/10.1093/brain/awf131 1210-1234 First published online: 1 June 2002

Summary

This report identifies evidence of partially functional cerebral regions in catastrophically injured brains. To study five patients in a persistent vegetative state (PVS) with different behavioural features, we employed [18F]fluorodeoxyglucose‐positron emission tomography (FDG‐PET), MRI and magnetoencephalographic (MEG) responses to sensory stimulation. Each patient’s brain expressed a unique metabolic pattern. In three of the five patients, co‐registered PET/MRI correlate islands of relatively preserved brain metabolism with isolated fragments of behaviour. Two patients had suffered anoxic injuries and demonstrated marked decreases in overall cerebral metabolism to 30–40% of normal. Two other patients with non‐anoxic, multifocal brain injuries demonstrated several isolated brain regions with relatively higher metabolic rates, that ranged up to 50–80% of normal. Nevertheless, their global metabolic rates remained <50% of normal. MEG recordings from three PVS patients provide clear evidence for the absence, abnormality or reduction of evoked responses. Despite major abnormalities, however, these data also provide evidence for localized residual activity at the cortical level. Each patient partially preserved restricted sensory representations, as evidenced by slow evoked magnetic fields and gamma band activity. In two patients, these activations correlate with isolated behavioural patterns and metabolic activity. Remaining active regions identified in the three PVS patients with behavioural fragments appear to consist of segregated corticothalamic networks that retain connectivity and partial functional integrity. A single patient who suffered severe injury to the tegmental mesencephalon and paramedian thalamus showed widely preserved cortical metabolism, and a global average metabolic rate of 65% of normal. The relatively high preservation of cortical metabolism in this patient defines the first functional correlate of clinical– pathological reports associating permanent unconsciousness with structural damage to these regions. The specific patterns of preserved metabolic activity identified in these patients do not appear to represent random survivals of a few neuronal islands; rather they reflect novel evidence of the modular nature of individual functional networks that underlie conscious brain function. The variations in cerebral metabolism in chronic PVS patients indicate that some cerebral regions can retain partial function in catastrophically injured brains.

  • Keywords: PET; MRI; consciousness; magnetoencephalography; persistent vegetative state
  • Abbreviations: AEF = auditory evoked magnetic field; CSPTC = corticostriatopallidal–thalamocortical; FDG‐PET = [18F]fluorodeoxyglucose‐positron emission tomography; MEF = magnetic evoked field; MEG = magnetoencephalography; PVS = persistent vegetative state; rCMRglu = regional cerebral metabolic rate for glucose; ROI = region (volume) of interest; SEF = somatosensory evoked magnetic field
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