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

  • Lijuan Cheng1,
  • Olivia Gosseries2,
  • Limei Ying1,
  • Xiaohua Hu3,
  • Dan Yu3,
  • Hongxing Gao3,
  • Minhui He1,
  • Caroline Schnakers2,
  • Steven Laureys2 and
  • Haibo Di1, 2Email author
Contributed equally
BMC NeurologyBMC series ¿ open, inclusive and trusted201313:27

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.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2377-13-27/MediaObjects/12883_2012_Article_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]).

Notes

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.

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