Abstract
Brain lesions can provide unique insight into the neuroanatomical substrate of human consciousness. For example, brainstem lesions causing coma map to a specific region of the tegmentum. Whether specific lesion locations outside the brainstem are associated with loss of consciousness (LOC) remains unclear. Here, we investigate the topography of cortical lesions causing prolonged LOC (N = 16), transient LOC (N = 91), or no LOC (N = 64). Using standard voxel lesion symptom mapping, no focus of brain damage was associated with LOC. Next, we computed the network of brain regions functionally connected to each lesion location using a large normative connectome dataset (N = 1,000). This technique, termed lesion network mapping, can test whether lesions causing LOC map to a connected brain circuit rather than one brain region. Connectivity between cortical lesion locations and an a priori coma‐specific region of brainstem tegmentum was an independent predictor of LOC (B = 1.2, p = .004). Connectivity to the dorsal brainstem was the only predictor of LOC in a whole‐brain voxel‐wise analysis. This relationship was driven by anticorrelation (negative correlation) between lesion locations and the dorsal brainstem. The map of regions anticorrelated to the dorsal brainstem thus defines a distributed brain circuit that, when damaged, is most likely to cause LOC. This circuit showed a slight posterior predominance and had peaks in the bilateral claustrum. Our results suggest that cortical lesions causing LOC map to a connected brain circuit, linking cortical lesions that disrupt consciousness to brainstem sites that maintain arousal.
Highlights
Consciousness depends on ascending projections from the dorsal brainstem that form what is commonly known as the ascending reticular activating system (Magoun, 1952)
We focused on connectivity between lesion locations and the dorsal brainstem given the established role of this region in supporting human consciousness (Fischer et al, 2016; Fuller, Sherman, Pedersen, Saper, & Lu, 2011; Hindman et al, 2018; Parvizi & Damasio, 2003)
We demonstrated a link between cortical lesions causing loss of consciousness (LOC) and arousal centers in the dorsal brainstem
Summary
Consciousness depends on ascending projections from the dorsal brainstem that form what is commonly known as the ascending reticular activating system (Magoun, 1952). Lesions causing a variety of different neuropsychiatric symptoms have recently been mapped to brain networks using a technique termed lesion network mapping (Boes et al, 2015; Darby, Laganiere, Pascual-Leone, Prasad, & Fox, 2017; Fasano, Laganiere, Lam, & Fox, 2017; Fischer et al, 2016; Fox, 2018; Laganiere, Boes, & Fox, 2016). With this technique, a large normative MRI database of resting-state functional connectivity (rsfcMRI) is used to identify brain regions functionally connected to each lesion location. We used voxel-wise statistics to map the exact location of the brainstem region most associated with LOC-producing lesions, and the functional network associated with this region
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