Elsevier

Brain and Cognition

Volume 77, Issue 3, December 2011, Pages 327-334
Brain and Cognition

Consciousness lost and found: Subjective experiences in an unresponsive state

https://doi.org/10.1016/j.bandc.2011.09.002Get rights and content

Abstract

Anesthetic-induced changes in the neural activity of the brain have been recently utilized as a research model to investigate the neural mechanisms of phenomenal consciousness. However, the anesthesiologic definition of consciousness as “responsiveness to the environment” seems to sidestep the possibility that an unresponsive individual may have subjective experiences. The aim of the present study was to analyze subjective reports in sessions where sedation and the loss of responsiveness were induced by dexmedetomidine, propofol, sevoflurane or xenon in a nonsurgical experimental setting. After regaining responsiveness, participants recalled subjective experiences in almost 60% of sessions. During dexmedetomidine sessions, subjective experiences were associated with shallower “depth of sedation” as measured by an electroencephalography-derived anesthesia depth monitor. Results confirm that subjective experiences may occur during clinically defined unresponsiveness, and that studies aiming to investigate phenomenal consciousness under sedative and anesthetic effects should control the subjective state of unresponsive participants with post-recovery interviews.

Highlights

► Subjective experiences occurred in 59% of sedative unresponsiveness sessions. ► Dexmedetomidine sedation had more subjective experiences than propofol sedation. ► Sevoflurane induced more laboratory related experiences than dexmedetomidine. ► Subjective experiences were related to shallower level of dexmedetomidine sedation.

Introduction

At present, no objective physiologic markers are known that would reveal with perfect accuracy the presence or the absence of consciousness. Therefore, in clinical medicine standardized scales of indirect behavioral criteria are typically used, such as the Glasgow Coma Scale (Teasdale & Jennett, 1974) or, more recently, the Full Outline of Unresponsiveness score (Wijdicks, Bamlet, Maramattom, Manno, & McClelland, 2005). Such scales rely on a patient’s behavioral responsiveness to standardized stimuli, e.g., a verbal command to open the eyes, or an application of a noxious stimulus. Typically, when meaningful behavioral responses to stimuli cannot be elicited, the person is defined as “unconscious”. Similarly, anesthesiologists use terms such as “loss of consciousness” to describe a state where a meaningful motor response to a verbal command, as well as explicit memory for the external events, is absent. Nevertheless, loss of motor response to a verbal stimulus merely represents disturbed control and interaction of these two brain functions. Typically, the additional criterion for “general anesthesia” is the loss of meaningful response to a painful stimulus, which usually takes place after the loss of responses to verbal stimuli and is therefore a state of deeper unconsciousness than the mere loss of responses to verbal commands.

In principle it is possible that someone who fulfills the criteria of being “unconscious” according to the above definition might still in another sense be “conscious”. That is, even a motorically unresponsive person may process information in other brain areas and thus might undergo, e.g., subjective experiences (either internally generated or triggered by external stimuli). The mere occurrence of subjective experiences is often called “phenomenal consciousness” (Block, 1995, Revonsuo, 2006). Phenomenal consciousness does not necessarily include the ability to respond to stimuli or communicate with the environment, as evidenced by the locked-in syndrome in which motor responses are lost but phenomenal consciousness is preserved (Kahane & Savulescu, 2009). Recently, also evidence from functional magnetic resonance imaging (fMRI) experiments with vegetative patients suggests that at least some of the patients undergo both internally generated and stimulus triggered subjective experiences, and are able to carry out mental imagery tasks according to the instructions given to them verbally (Monti et al., 2010, Owen et al., 2006).

In consciousness research, a new concept has been recently introduced to refer to the dissociation between the first and the second type of consciousness (responsiveness vs. phenomenal consciousness). A person who fulfills the criteria of “unconsciousness” based on external responsiveness (e.g., to verbal commands) despite the fact that he or she is phenomenally conscious, is called an “inverse zombie” (Mashour & LaRock, 2008). In anesthesiology, a state of “inversed zombiehood” with preserved phenomenal consciousness during anesthetically induced unconsciousness has been studied under the labels of “anesthesia awareness” and “anesthesia dreaming” (Errando et al., 2008). The former concept refers to veridical awareness of external stimuli during the unresponsive state, the latter to the occurrence of purely internally generated, stimulus-independent subjective experiences during the unresponsive state.

Studies on surgical patients have shown that anesthesia awareness is a relatively rare, but still occasionally occurring condition with estimated frequencies ranging from 0.023% to 1% of the general anesthesia cases (Errando et al., 2008, Mashour et al., 2009, Ranta et al., 1998, Sandin et al., 2000), with a common reported incidence being around 0.13% (Sebel et al., 2004; for discussion regarding different incidence estimates, see Sebel, 2009). The occurrence of anesthesia dreaming appears to be a much more common phenomenon, and has been reported in 6–53% of post-anesthesia interviews (Brandner et al., 1997, Errando et al., 2008, Leslie et al., 2007, Leslie et al., 2005). The exact incidence is, however, very difficult to estimate, because it depends on several intervening factors, such as the length and the depth of anesthesia required for different medical interventions, the way in which the patients are interviewed about their experiences, and the delay between the recovery from anesthesia and the interview. Furthermore, the patients’ general medical condition as well as combination of various anesthetic agents and other drugs given during surgery may affect the memory and reduce recall for such experiences.

In the present study our main aim was to specifically estimate the frequency of the occurrence of subjective experiences during sedative “unconsciousness” as defined by the loss of behavioral responsiveness to verbal stimuli. In addition, the following research questions were asked: What kinds of contents of phenomenal consciousness are reported and what is the frequency of their recall? Does the recall frequency of subjective experiences depend on the type of sedative/anesthetic agent used? Does the recall frequency of subjective experiences depend on the “depth of sedation” as measured by an electroencephalography (EEG)-derived anesthesia depth monitor? The study was designed to avoid many of the problems of previous studies. First, we used only young healthy participants without any notable cognitive or memory problems. Second, the setting was completely experimental rather than clinical or surgical. Third, we used single sedative/anesthetic agents rather than drug cocktails. Fourth, no other drugs in addition to the sedative/anesthetic were applied (such as muscle relaxants). Fifth, the behavioral loss of consciousness was carefully tested throughout the sessions, which is not common in clinical settings. Sixth, the “depth of sedation” was conscientiously monitored by an EEG-derived measure. Seventh, after the session the participants were interviewed twice in detail using a structured interview specifically inquiring about their subjective experiences during the state of unresponsiveness. Eighth, the content of the participants’ reports and the quality of the subjective experiences was analyzed in detail by methods similar to those used in dream research to study dream reports. Thus, we expected to develop a more systematic and accurate description of dissociation between phenomenal consciousness and behavioral unresponsiveness than many of the previous studies have been able to provide.

Section snippets

Participants

An open invitation for students to participate in the study, which was designed to explore the neural mechanisms of the loss of responsiveness, was put to several notice boards at the campus area as well as to the intranet pages of the University of Turku. Forty right-handed male volunteers, age 18–30 years, signed an informed consent and were paid for participation in the study. All participants were of a good general health (American Society of Anesthesiologists physical status I). The study

Incidence of subjective experiences

After ROR, subjective experiences were reported in 62.5% of sessions when unresponsiveness was induced for the first time (N = 40), in 50% of sessions when unresponsiveness was induced for the second time (N = 18), and taken together, in 58.6% of all sessions (N = 58) (see Table 2). During the first sessions, the difference between the frequency of reports with subjective experiences across all four anesthetic groups was not significant (N = 40, p = .057, Fisher’s exact test). When drugs were compared

Discussion

Results of the present study show that unresponsiveness to verbal stimuli caused by different sedative/anesthetic agents is frequently accompanied by subjective experiences, ranging from simple sensations to complex dream-like stories. This finding extends observation of the presence of subjective experiences in otherwise unresponsive vegetative patients (Monti et al., 2010, Owen et al., 2006) to anesthetic-induced loss of responsiveness in healthy participants, which has important implications

Acknowledgments

This work was supported by the Academy of Finland (Projects 8110957, 8111818, 8124623), the Signe and Ane Gyllenberg Foundation, and the National Graduate School of Psychology in Finland.

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