Assessment of localisation to auditory stimulation in post-comatose states: use the patient’s own name

  • Lijuan Cheng1Email author,

    Affiliated with

    • Olivia Gosseries2Email author,

      Affiliated with

      • Limei Ying1,

        Affiliated with

        • Xiaohua Hu3,

          Affiliated with

          • Dan Yu3,

            Affiliated with

            • Hongxing Gao3,

              Affiliated with

              • Minhui He1,

                Affiliated with

                • Caroline Schnakers2,

                  Affiliated with

                  • Steven Laureys2 and

                    Affiliated with

                    • Haibo Di1, 2Email author

                      Affiliated with

                      BMC Neurology201313:27

                      DOI: 10.1186/1471-2377-13-27

                      Received: 7 December 2012

                      Accepted: 11 March 2013

                      Published: 18 March 2013

                      Abstract

                      Background

                      At present, there is no consensus on how to clinically assess localisation to sound in patients recovering from coma. We here studied auditory localisation using the patient’s own name as compared to a meaningless sound (i.e., ringing bell).

                      Methods

                      Eighty-six post-comatose patients diagnosed with a vegetative state/unresponsive wakefulness syndrome or a minimally conscious state were prospectively included. Localisation of auditory stimulation (i.e., head or eyes orientation toward the sound) was assessed using the patient’s own name as compared to a ringing bell. Statistical analyses used binomial testing with bonferroni correction for multiple comparisons.

                      Results

                      37 (43%) out of the 86 studied patients showed localisation to auditory stimulation. More patients (n=34, 40%) oriented the head or eyes to their own name as compared to sound (n=20, 23%; p<0.001).

                      Conclusions

                      When assessing auditory function in disorders of consciousness, using the patient’s own name is here shown to be more suitable to elicit a response as compared to neutral sound.

                      Keywords

                      Localisation to sound Auditory localisation Vegetative state Unresponsive wakefulness syndrome Minimally conscious state Own name Disorders of consciousness

                      Background

                      At present, there is no consensus on what auditory stimulus should be employed for the assessment of localisation to sound in disorders of consciousness such as the “vegetative state” (now also coined unresponsive wakefulness syndrome; VS/UWS [1]) and the minimally conscious state (MCS) [2]. Indeed, several behavioural “coma scales” use different stimuli to evaluate auditory localisation. For instance, the Coma Recovery Scale-Revised (CRS-R), the Sensory Modality Assessment Rehabilitation Technique and the Western Neuro-Sensory Stimulation Profile leave the choice open between several auditory stimuli (e.g., noise, voice). The Coma/Near Coma Scale requests to use “5s of bell ringing”, and the Wessex Head Injury Matrix uses a noise (bell, whistle or buzzer) and “a person talking” (for a review, see [3]).

                      We here propose to use the patient’s own name (as compared to a meaningless noise) in the assessment of localisation to sound. The own name is intrinsically meaningful for each of us because of its personal significance, emotional content and repetition along life. Beyond our day-to-day experience, the extreme salience of being presented one's own name was highlighted in various experimental and clinical studies. Some of these suggest that self-referential stimuli are so potent that they can "capture attention and subsequently bring the stimulus into awareness" [4]. In everyday social interactions, auto-referential stimuli give rise to a sense of self-awareness, as reflected in the cocktail party phenomenon when hearing our own name [5]. This particularly easy detection in usual laboratory experiments with healthy participants is consistent with research that showed powerful detection of the own name in situations of reduced consciousness [6, 7]. The aim of the present study is to determine whether the assessment of localisation to sound in patients recovering from coma is influenced by the choice of the auditory stimulus.

                      Methods

                      Eighty-six patients recovering from coma were prospectively assessed free of sedative drugs. Each patient was studied in a sitting position and a standardized arousal facilitation protocol (i.e., deep pressure stimulations from the facial musculature to the toes) was employed if needed in order to prolong the length of time the patient maintained arousal [8]. Localisation to sound was evaluated using a standardized methodology as described in the CRS-R [8]. In brief, an auditory stimulus (bell and patient’s own name) was presented from the right and from the left side while the examiner stood next to the patient but out of view. Stimuli were matched for intensity and duration of presentation, and were presented twice for each side. The order of presentation was randomized using “random number” procedure in Excel. Localisation to auditory stimulation was defined as head or eyes orientation toward the location of the stimulus on both trials for at least one side. Special care was made not to present stimuli when spontaneous eye or head movements were occurring. Clinical diagnosis was made according to the Aspen workgroup criteria for disorders of consciousness [2] and based on the CRS-R assessments [8] performed by two trained and experienced neuropsychologists. Note that according to these guidelines auditory localisation is compatible with the diagnosis of VS/UWS. The study was approved by the Ethics Committee of Hangzhou Normal University and Wujing Hospital which complies with the Code of Ethics of the World Medical Association (Declaration of Helsinki). Informed consents were obtained by the patient’s legal surrogates.

                      Differences between localisation as assessed by bell or patient's own name were measured using binomial testing (Stata Statistical Software; Release 11.2. College Station, TX: StataCorp LP 2009). Bonferroni correction was applied for multiple comparisons. Results were considered significant at p<0.01.

                      Results

                      Out of 86 patients (67 men; mean age 46 (SD 17) years), 47 (55%) were diagnosed in VS/UWS [1] and 37 (45%) were in MCS. Median time between injury and assessment was 5 months (IQR: 3 – 13 months). Aetiology was traumatic in 53 (61%) and non-traumatic in 33 (39%) patients. 37 (43%) out of the 86 studied patients showed localisation to auditory stimulation. Overall, more patients (n=34, 40%) oriented the head or eyes to the own name as compared to sound (n=20, 23%; p<0.001) (Table 1). MCS patients localized more often to their own name as compared to sound (p<0.001). This effect was not significant in the VS/UWS group (p>0.05) (Figure 1).
                      Table 1

                      Auditory localisation according to diagnosis and aetiology

                      Diagnosis

                      Localisation response

                      Aetiology

                      Total

                       

                      Own name

                      Bell

                      Both

                      None

                      Traumatic

                      Non traumatic

                       

                      VS/UWS

                      4 (5%)

                      1 (1%)

                      4 (5%)

                      38 (44%)

                      26 (30%)

                      21 (25%)

                      47

                      MCS

                      13 (15%)

                      2 (2%)

                      13 (15%)

                      11 (13%)

                      27 (31%)

                      12 (14%)

                      39

                      Total

                      17 (20%)

                      3 (3%)

                      17 (20%)

                      49 (57%)

                      53 (61%)

                      33 (39%)

                      86

                      Number of patients showing localisation to the own name, ringing bell or both as a function of diagnosis [vegetative state (VS/UWS) versus minimally conscious state (MCS)] and aetiology.

                      http://static-content.springer.com/image/art%3A10.1186%2F1471-2377-13-27/MediaObjects/12883_2012_749_Fig1_HTML.jpg
                      Figure 1

                      Auditory localisation. Number of patients in vegetative/unresponsive state (VS/UWS) and minimally conscious state (MCS) showing localisation to sound (n=37) as a function of the employed stimulus (own name in black and ringing bell in white).

                      Tables 2 and 3 show the clinical data for each patient (MCS and VS/UWS patient groups respectively). Localisation preference was not different depending on aetiology or time since insult (p>0.05). The overall behavioural responsiveness assessed by the CRS-R total score tended to be higher when patients localized both stimuli than when they did not show any localisation (Tables 2 and 3). For instance, MCS patients showing both responses to their own name and to the bell had a CRS-R total score between 9 and 18 whereas MCS patients showing no localisation had a score between 6 and 10. Patients localizing to their own name only (or bell only) showed intermediate CRS-R total scores. In the 37 patients showing localisation, 9 patients were considered as being in VS/UWS according to the CRS-R criteria (i.e., they showed no response to command, no orientation to pain and no visual tracking) - 4 of these patients showed orientation to the own name but not to sound.
                      Table 2

                      Clinical data of the MCS patients

                      Patient

                      Gender

                      Aetiology

                      Time since injury*

                      CRS-R score**

                      Auditory localisation

                      MCS1

                      male

                      trauma

                      7

                      6

                      none

                      MCS2

                      male

                      trauma

                      73

                      7

                      none

                      MCS3

                      male

                      trauma

                      21

                      7

                      none

                      MCS4

                      female

                      trauma

                      20

                      7

                      none

                      MCS5

                      male

                      trauma

                      155

                      8

                      none

                      MCS6

                      female

                      trauma

                      160

                      8

                      none

                      MCS7

                      female

                      trauma

                      21

                      8

                      none

                      MCS8

                      male

                      trauma

                      205

                      9

                      none

                      MCS9

                      male

                      trauma

                      20

                      10

                      none

                      MCS10

                      male

                      stroke

                      51

                      10

                      none

                      MCS11

                      male

                      trauma

                      45

                      10

                      none

                      MCS12

                      female

                      trauma

                      9

                      8

                      bell

                      MCS13

                      male

                      stroke

                      32

                      9

                      bell

                      MCS14

                      male

                      trauma

                      55

                      8

                      own name

                      MCS15

                      male

                      trauma

                      11

                      8

                      own name

                      MCS16

                      male

                      trauma

                      221

                      8

                      own name

                      MCS17

                      male

                      trauma

                      150

                      9

                      own name

                      MCS18

                      male

                      trauma

                      40

                      9

                      own name

                      MCS19

                      female

                      stroke

                      14

                      9

                      own name

                      MCS20

                      male

                      stroke

                      61

                      10

                      own name

                      MCS21

                      male

                      trauma

                      22

                      10

                      own name

                      MCS22

                      male

                      trauma

                      19

                      13

                      own name

                      MCS23

                      male

                      trauma

                      7

                      13

                      own name

                      MCS24

                      female

                      trauma

                      54

                      14

                      own name

                      MCS25

                      male

                      trauma

                      291

                      14

                      own name

                      MCS26

                      male

                      stroke

                      115

                      16

                      own name

                      MCS27

                      male

                      anoxia

                      50

                      9

                      both

                      MCS28

                      female

                      trauma

                      7

                      10

                      both

                      MCS29

                      male

                      trauma

                      13

                      10

                      both

                      MCS30

                      male

                      trauma

                      121

                      10

                      both

                      MCS31

                      male

                      trauma

                      33

                      11

                      both

                      MCS32

                      male

                      stroke

                      13

                      11

                      both

                      MCS33

                      male

                      trauma

                      12

                      12

                      both

                      MCS34

                      male

                      stroke

                      9

                      13

                      both

                      MCS35

                      female

                      stroke

                      22

                      15

                      both

                      MCS36

                      male

                      anoxia

                      135

                      16

                      both

                      MCS37

                      male

                      stroke

                      6

                      16

                      both

                      MCS38

                      male

                      anoxia

                      57

                      17

                      both

                      MCS39

                      male

                      trauma

                      3

                      18

                      both

                      *Time since injury in weeks, ** Total score of the Coma Recovery Scale-Revised (minimum 0, maximum 23).

                      Table 3

                      Clinical data of the VS/UWS patients

                      Patient

                      Gender

                      Aetiology

                      Time since injury*

                      CRS-R score**

                      Auditory localisation

                      VS/UWS1

                      male

                      stroke

                      9

                      2

                      none

                      VS/UWS2

                      male

                      anoxic

                      6

                      3

                      none

                      VS/UWS3

                      male

                      trauma

                      34

                      3

                      none

                      VS/UWS4

                      male

                      trauma

                      17

                      3

                      none

                      VS/UWS5

                      male

                      stroke

                      66

                      4

                      none

                      VS/UWS6

                      male

                      anoxic

                      82

                      4

                      none

                      VS/UWS7

                      male

                      trauma

                      39

                      4

                      none

                      VS/UWS8

                      male

                      trauma

                      13

                      4

                      none

                      VS/UWS9

                      female

                      anoxia

                      4

                      4

                      none

                      VS/UWS10

                      male

                      stroke

                      13

                      5

                      none

                      VS/UWS11

                      male

                      anoxia

                      89

                      5

                      none

                      VS/UWS12

                      male

                      stroke

                      5

                      5

                      none

                      VS/UWS13

                      female

                      trauma

                      8

                      5

                      none

                      VS/UWS14

                      male

                      trauma

                      189

                      5

                      none

                      VS/UWS15

                      female

                      stroke

                      5

                      5

                      none

                      VS/UWS16

                      male

                      stroke

                      3

                      5

                      none

                      VS/UWS17

                      female

                      trauma

                      68

                      6

                      none

                      VS/UWS18

                      male

                      trauma

                      76

                      6

                      none

                      VS/UWS19

                      male

                      trauma

                      36

                      6

                      none

                      VS/UWS20

                      male

                      trauma

                      13

                      6

                      none

                      VS/UWS21

                      male

                      trauma

                      22

                      6

                      none

                      VS/UWS22

                      male

                      trauma

                      8

                      6

                      none

                      VS/UWS23

                      male

                      stroke

                      21

                      6

                      none

                      VS/UWS24

                      male

                      trauma

                      9

                      6

                      none

                      VS/UWS25

                      male

                      stroke

                      16

                      6

                      none

                      VS/UWS26

                      male

                      trauma

                      34

                      6

                      none

                      VS/UWS27

                      male

                      trauma

                      19

                      6

                      none

                      VS/UWS28

                      male

                      trauma

                      12

                      6

                      none

                      VS/UWS29

                      female

                      stroke

                      11

                      6

                      none

                      VS/UWS30

                      male

                      trauma

                      70

                      6

                      none

                      VS/UWS31

                      male

                      anoxia

                      413

                      6

                      none

                      VS/UWS32

                      male

                      trauma

                      28

                      6

                      none

                      VS/UWS33

                      male

                      trauma

                      34

                      7

                      none

                      VS/UWS34

                      male

                      trauma

                      24

                      7

                      none

                      VS/UWS35

                      female

                      trauma

                      11

                      7

                      none

                      VS/UWS36

                      male

                      stroke

                      9

                      7

                      none

                      VS/UWS37

                      female

                      stroke

                      13

                      7

                      none

                      VS/UWS38

                      male

                      trauma

                      10

                      7

                      none

                      VS/UWS39

                      female

                      anoxic

                      16

                      4

                      bell

                      VS/UWS40

                      male

                      anoxic

                      557

                      8

                      bell

                      VS/UWS41

                      male

                      stroke

                      39

                      5

                      own name

                      VS/UWS42

                      female

                      trauma

                      18

                      6

                      own name

                      VS/UWS43

                      male

                      anoxia

                      23

                      7

                      own name

                      VS/UWS44

                      female

                      anoxia

                      15

                      7

                      own name

                      VS/UWS45

                      female

                      trauma

                      20

                      6

                      both

                      VS/UWS46

                      male

                      trauma

                      14

                      7

                      both

                      VS/UWS47

                      male

                      trauma

                      38

                      8

                      both

                      *Time since injury in weeks, **Total score of the Coma Recovery Scale-Revised (minimum 0, maximum 23).

                      Discussion

                      Our data show that the assessment of localisation to sound depends on what stimulus is employed. MCS patients tend to best orient to their own name as compared to a meaningless loud sound (i.e., ringing bell). Indeed, one’s own name is a piece of information that we use to process in the auditory modality from infancy: 4–5 month-old infants are able to recognize the sound pattern of their own names [9]. In end-stage demented patients, it has also been shown that perception of the own name deteriorates well after perception of time, place and recognition [10]. Similarly, after general anaesthesia, the patient’s reactivity to the own name occurs first, before reactivity to pain and noise [11]. In MCS patients, clinical experience learns that behavioural responses to auto-referential stimuli such as the own face are amidst the first signs heralding further recovery of consciousness [12]. Event-related potential studies have also shown that hearing one’s own name, as compared to meaningless noise, leads to an increased mismatch negativity response in patients with disorders of consciousness [6]. In addition, functional MRI studies assessing brain activation to the own name have reported activation of “self”-related brain regions (i.e., anterior cingulate and mesiofrontal cortices) depending of the level of consciousness in patients recovering from coma [7, 13].

                      28% of the studied MCS patients (11/39) failed to show auditory localisation. Neurological assessment showed that 2 of these 11 patients (18%) had absent auditory startle, while 9 (82%) showed auditory-independent signs of consciousness. In line with previous studies, auditory impairment probably explains this finding [3].

                      Auditory localisation seems to be related to the patient’s overall behavioural responsivity: the more the patients are conscious, the more they tend to respond to both auditory stimuli. Moreover, our results showed that most of the patients who responded to the bell also responded to their own name (condition “both” in Table 1). Three patients however showed localisation to the bell but not to their own name. Even if they retained basic auditory processing, these three patients might not have been able to process language, and hence recognize their own name. Another explanation could be the presentation of the patient's own name as last stimulus, and hence fatigue might explain orientation to a bell in the absence of orientation to the own name.

                      One should note that the duration and the degree of the movement towards auditory stimulation were not taken into account to assess auditory localisation (as described in the CRS-R). This should nevertheless be investigated in future studies to allow differentiating between a brief movement and a sustained fixation following auditory stimulation. Indeed, the latter may potentially be considered as a sign of consciousness, as it is the case for visual and tactile localisation (e.g., visual pursuit and localisation to noxious stimulation items in the CRS-R). Such responses may also be worth exploring further using neuroimaging techniques such as fMRI and EEG in order to compare the behavioral responses and the underlying cerebral networks involved when hearing the person's name being called.

                      Conclusions

                      Our findings emphasize the clinical importance of using the patient's own name when performing bedside testing of localisation to sound, adding to previous studies the importance of using auto-referential stimuli in patients with disorders of consciousness (i.e., the use of a mirror in the assessment of visual tracking [12]).

                      Abbreviations

                      VS/UWS: 

                      Vegetative state/unresponsive wakefulness syndrome

                      MCS: 

                      Minimally conscious state

                      CRS-R: 

                      Coma recovery scale-revised

                      fMRI: 

                      Functional magnetic resonance imaging

                      EEG: 

                      Electroencephalography.

                      Declarations

                      Acknowledgements

                      This study was supported by the National Natural Science Foundation of China (30870861), the Science and Technology Department of Zhejiang Province (2008C14098), the Hangzhou Normal University and HNUEYT, the Belgian Funds for Scientific Research (FNRS), Fonds Léon Frédericq, and the University of Liège. The authors thank Cunlai Xu, Jian Gao, Kehong Liu, Kun Li,Yu Zhang, Hongyan Song and Yan Dong for their assistance in patients’ assessment, and Didier Ledoux for his statistical advices. OG and CS are postdoctoral researchers and SL is research director at FNRS.

                      Authors’ Affiliations

                      (1)
                      International Vegetative State and Consciousness Science Institute, Hangzhou Normal University
                      (2)
                      Coma Science Group, Cyclotron Research Centre and Neurology Department, University and University Hospital of Liege
                      (3)
                      Rehabilitation Center for Brain Damage, Wujing Hospital of Hangzhou City

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                      14. Pre-publication history

                        1. The pre-publication history for this paper can be accessed here:http://​www.​biomedcentral.​com/​1471-2377/​13/​27/​prepub

                      Copyright

                      © Cheng et al.; licensee BioMed Central Ltd. 2013

                      This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://​creativecommons.​org/​licenses/​by/​2.​0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.