The vegetative state (VS) is characterized by a preserved arousal level but also by the absence of any sign of consciousness of the environment and of oneself (e.g., absence of oriented responses to environmental stimulation) (The Multi-Society Task Force on PVS 1994). The patient in a minimally conscious state (MCS), on the contrary, demonstrates inconsistent, basic but reproducible signs of consciousness of the environment and of oneself (e.g., oriented responses to environmental stimulation suggesting an interaction between the patient and his/her surroundings) (Giacino et al. Reference Giacino, Ashwal, Childs, Cranford, Jennett, Katz, Kelly, Rosenberg, Whyte and Zafonte2002). Both populations may be particularly useful for studying the concept of consciousness via the progressive recovery of the most primary aspects of consciousness, and the behavioral and cerebral correlates that accompany them.

Niedenthal et al. discuss the importance of eye gaze in embodied simulation and, more globally, in the processing of emotional visual stimulation (such as facial expression). Eye gaze involves interaction between the subject and his/her surroundings. At a neurobehavioral level, oriented eye movements are usually associated with conscious processing (Giacino et al. Reference Giacino, Ashwal, Childs, Cranford, Jennett, Katz, Kelly, Rosenberg, Whyte and Zafonte2002). MCS patients are able to track a person moving in front of them, whereas VS patients are not. Only MCS patients can therefore detect emotional visual stimuli present in their surroundings. According to a recent study, visual pursuit is more frequently detected in response to emotional stimulation (e.g., the appearance of one's face in a mirror) than to non-emotional stimulation (e.g., a person moving) (Vanhaudenhuyse et al. Reference Vanhaudenhuyse, Schnakers, Bredart and Laureys2008).

MCS patients also show more complex emotional responses than VS patients. For instance, VS patients may smile or grimace, shed tears, or make grunting or groaning sounds, but for no discernible reason (The Multi-Society Task Force on PVS 1994; Working Party of the Royal College of Physicians 2003), similarly to what can be observed in anencephalic infants lacking a functional neocortex (Massimelli Reference Massimelli2007). MCS patients can manifest appropriate smiling or crying in response to specific linguistic or visual content of emotional stimuli, suggesting an appropriate interaction between the patient and his/her environment (Giacino et al. Reference Giacino, Ashwal, Childs, Cranford, Jennett, Katz, Kelly, Rosenberg, Whyte and Zafonte2002). Here, consciousness is reflected by the presence of basic but contingent social and emotional behaviors, those requiring a complex cortical activity. Using auditory (Laureys et al. Reference Laureys, Faymonville, Degueldre, Fiore, Damas, Lambermont, Janssens, Aerts, Franck, Luxen, Moonen, Lamy and Maquet2000) and noxious stimuli (Boyl et al. 2008; Laureys et al. Reference Laureys, Faymonville, Peigneux, Damas, Lambermont, Del Fiore, Degueldre, Aerts, Luxen and Franck2002), previous studies in functional neuroimaging have shown that, while brain activation isolated to primary cortices is observed in VS patients, an activation in associative areas as well as preserved functional connectivity between cortico-cortical areas (i.e., between primary and associative cortices) is observed in MCS patients (see our Fig. 1). MCS patients seem, therefore, to present a more complex social and emotional pattern at a behavioral level and a more integrative brain processing than VS patients.

Figure 1.

Cerebral activation to noxious stimulation. In the darker brain regions (which appear in red in the online version, available at www.journals.cambridge.org/bbs) that activated more during noxious stimulation in healthy controls (top), in vegetative state (bottom, left side) and in minimally conscious state (bottom, right side) as compared to rest (adapted from Boly et al. Reference Boly, Faymonville, Schnakers, Peigneux, Lambermont, Phillips, Lancellotti, Luxen, Lamy, Moonen, Maquet and Laureys2008 and Laureys et al. Reference Laureys, Faymonville, Peigneux, Damas, Lambermont, Del Fiore, Degueldre, Aerts, Luxen and Franck2002).

Even if oriented eye movements, such as visual pursuit, are usually considered a sign of consciousness, controversies remain concerning visual fixation. Visual fixation includes eye gaze and can be described as the eyes changing from their initial fixation point and refixating on the new target location (Giacino et al. Reference Giacino, Kalmar and Whyte2004). As eye gaze involves interaction between the subject and his/her surroundings, visual fixation would have to be considered as a sign of consciousness. However, whereas the Aspen Workgoup considers this behavior as a sign of consciousness (Giacino et al. Reference Giacino, Ashwal, Childs, Cranford, Jennett, Katz, Kelly, Rosenberg, Whyte and Zafonte2002), the College of Physicians considers its presence as reflecting a reflexive activity (Working Party of the Royal College of Physicians 2003). Using active paradigms (i.e., the patients were asked to mentally perform a task), voluntary brain activity has been obtained in patients showing mainly low-level behavioral responses such as visual fixation, suggesting it may be a sign of consciousness (Owen et al. Reference Owen, Coleman, Boly, Davis, Laureys and Pickard2006; Schnakers et al. Reference Schnakers, Perrin, Schabus, Majerus, Ledoux, Damas, Boly, Vanhaudenhuyse, Bruno, Moonen and Laureys2008). However, we have recently shown no differences in brain activity and connectivity in VS patients presenting or not presenting visual fixation, suggesting that it does not necessarily reflect consciousness and higher-order cortical functioning (Bruno et al. Reference Bruno, Vanhaudenhuyse, Schnakers, Boly, Gosseries, Demertzi, Majerus, Moonen, Hustinx and Laureys2010). According to these results, it is not clear whether visual fixation reflects conscious interaction between the patient and his/her surroundings.

In conclusion, consciousness level is associated with social and emotional behaviors of different complexity. Conscious patients (i.e., MCS) show high-level behavioral responses and brain activation as compared to non-conscious patients (i.e., VS). Nevertheless, the particular case of visual fixation would have to be further investigated in order to better define its relationship to consciousness.