Near-Infrared Spectroscopy to Assess Covert Volitional Brain Activity in Intensive Care

Abstract

Background: Detecting covert consciousness in unresponsive patients is challenging. Although functional magnetic resonance imaging and advanced electroencephalography paradigms can identify volitional brain activity, the limited accessibility of these technologies necessitates alternative approaches. Functional near-infrared spectroscopy may provide a portable solution in the intensive care unit. We assessed the feasibility of functional near-infrared spectroscopy with verbal motor commands to detect volitional brain activity in acute disorders of consciousness (DoC).

Methods: Functional near-infrared spectroscopy recordings and clinical assessments were obtained from 50 patients with DoC with acute brain injury, with data analyzed post hoc and visually at the bedside. Twenty healthy volunteers served as controls.

Results: After quality control, data from 19 controls and 36 patients were analyzed. Cortical activation was detected in 18 (96%) controls and 16 (44%) patients. Among 13 minimally conscious patients, volitional activity was found in 8 (62%), whereas 8 (35%) of 23 clinically unresponsive patients showed activation. Volitional brain activity in the latter was associated with higher odds of command following within a week, although it was not statistically significant (odds ratio 3.1, 95% confidence interval 0.7-15.8; p = 0.14). Visual bedside analysis showed high specificity (90%) but moderate agreement (κ = 0.4) with post hoc computational analysis.

Conclusions: Functional near-infrared spectroscopy with motor commands can detect volitional brain activity in acute DoC, although data quality issues remain a limitation.

Keywords: Brain injury; Cognitive motor dissociation; Coma; Consciousness; Neuromonitoring; Prognostication.

Fig. 1

Montage for functional near-infrared spectroscopy data acquisition. The left panel displays a topographic optode layout on a standard 10–10 coordinate system, in which red circles represent sources (S01–S08) and blue circles represent detectors (D01–D07). Optodes were positioned over the frontal cortex, supplementary motor areas, tongue motor homunculi, and parietal cortex, with short-channel detectors placed directly under each source. The right panel shows a 3D reconstruction of the optode placement on a head model, illustrating the spatial arrangement of sources and detectors. Illustrations created in NIRSite and Aurora systems, shown with permission by NIRx Medical system, Berlin, Germany

Fig. 2

Functional near-infrared spectroscopy time series of two study participants demonstrating volitional brain activity. Three-dimensional cortical maps show task-related cortical activation during a motor task in a healthy control (a, identifier [ID] 13 in Fig. 1) and a clinically comatose patient (b, ID 7 in Fig. 2). Time series plots display changes in oxyhemoglobin (HbO) (red) and deoxyhemoglobin (HbR) (blue) concentrations across task (tongue motor command) and rest blocks. In the tongue motor homunculus, tongue motor command blocks show a pattern of increased HbO and decreased HbR, consistent with volitional activation (the first block from the left), whereas all other blocks show no significant hemodynamic changes and hence no task-related activations. Shaded areas represent the standard error of the mean

Fig. 3

Brain activation patterns in healthy controls during the tongue motor command task. A 3D visualization of cortical regions activated during motor command compared with rest periods from 19 healthy volunteers. Regions highlighted in red indicate channels with significant cortical activation. Activation is predominantly observed in the supplementary motor area, followed by frontal regions and tongue motor cortex

Fig. 4

Cortical activation patterns in clinically unresponsive patients during tongue motor commands. Regions highlighted in red indicate significant volitional cortical activation during the task compared to rest, suggesting that these clinically unresponsive patients were in a state of cognitive motor dissociation. Decimal notations indicate the sequence of recordings for patients with multiple assessments. Activation is predominantly observed in the tongue motor cortex, followed by the supplementary motor area and frontal regions. Numbers indicate patient identifiers corresponding to Table S2. *Patients 29 and 36 had progressed to MCS + and eMCS, respectively, during repeated near-infrared spectroscopy evaluation. #Patients who regained command following within 1 week. eMCS, emerging from minimally conscious state, MCS, minimally conscious state, MCS + , minimally conscious state–positive, UWS, unresponsive wakefulness syndrome

Fig. 5

Cortical activation patterns in clinically low-responsive patients during tongue motor commands. Regions highlighted in red indicate significant cortical activation during the task compared with rest. Decimal notations indicate the sequence of recordings for patients with multiple assessments. Numbers indicate patient identifiers corresponding to Table S2. #Patients who regained command following within 1 week. eMCS, emerging from minimally conscious state, MCS, minimally conscious state, MCS − , minimally conscious state–negative, MCS + , minimally conscious state–positive, UWS, unresponsive wakefulness syndrome