You are on page 1of 3

02007 VOL. 38 NO.

CLINICAL EEG and NEUROSCIENCE

Recognizing a Mother's Voice


in the Persistent Vegetative State
C. Machado, J. Korein, E. Aubert, J. Bosch, M. A. Alvarez, R. Rodriguez,
P. Valdes, L. Portela, M. Garcia, N. Perez, M. Chinchilla, Y. Machado and Y. Machado

MATERIALS AND METHODS


We studied an 8-year-old boy after a near-drowning left
him in a VS for 4 years before the study. Findings fulfilled
all clinical criteria for the diagnosis of VS. Diagnostic criteria for VS include: eye movements with lack of fixation, lack
of evidence of awareness of self or environment, lack of
interaction with others, and lack of comprehension or
expression of language. Often stimuli result in massive
stretching or startle reactions, without proper habituation,
showing sometimes massive flexing responses. In our
case, occasionally grimacing occurred after stimulation.
Nonetheless, external stimuli did not evoke purposeful or
sustained and reproducible voluntary behavioral responses. Hence, we definitely diagnosed our patient as a case of
persistent vegetative state (PVS).a
The data were assessed using quantitative electric
tomography (QEEGt), a technique that combines anatomical information of the brain by MRI with EEG patterns, to
estimate the sources of the EEG within the brain.9-11
The EEG was recorded using nineteen monopolar derivations of the International 10-20 System (FPI, FP2, F3,
F4, C3, C4, P3, P 4 , 0 1 , 0 2 , F7, F8, T3, T4, T5, T6, Fz, Cz,
Pz) with linked earlobes as a reference. Eye movement
artifacts were monitored by use of the electrooculogram
(EOG). The data acquisition was performed using a MEDICID-05 System (Neuronic S.A.). After visual editing to
remove artifacts, 45 artifact-free samples were selected,
each 2.5 seconds long, for each experimental condition,
and were transformed using the FFT to the frequency
domain, yielding a power spectrum from 0.78 to 70 Hz with
a sampling frequency of 0.39 Hz (178 frequencies), with a
60 Hz notch filter.10
The Variable Resolution Electrical Tomography (VARETA) method was used for estimating EEG source genera-

Key Words
Consciousness Awareness
Electroencephalography
Gamma Coherence
Persistent Vegetative State
Quantitative Electric Tomography
Vegetative State
ABSTRACT
We studied an 8-year-old boy after a neardrowning left
him in a vegetative state (VS) for 4 years before the study.
Findings fulfilled all clinical criteria for the diagnosis of VS.
The purpose of this study was to investigate whether there
was significant differential activation of the brain in
response to hearing his mother's voice compared with the
voices of unknown women. The data were assessed using
quantitative electric tomography (QEEGt), a technique that
combines anatomical information of the brain by MRI with
EEG patterns to estimate the sources of the EEG within the
brain. We found significant differences for EEG frequencies from 14-58 Hz, with a peak at 33.2 Hz (gamma band).
The 3D reconstruction showed that these statistical differences were localized in the lateral and posterior regions of
the left hemisphere. No significant differences were found
between unknown women vs. basal conditions. These
results demonstrate recognition of the mother's voice and
indicate high-level residual linguistic processing in a
patient meeting clinical criteria for VS. These findings
launch new ethical and practical implications for the management of VS patients.
INTRODUCTION
The diagnosis of vegetative state (VS) has been made
more difficult by recognition of the minimally conscious
state (MCS) as a transitional phase in the partial recovery
of self-awareness or environmental awareness while
emerging from the VS, leading to a relative high proportion
of errors.' 5 Neuroimaging techniques have provided new
insights for the pathophysiological elucidation of consciousness generation in these cases.267
The purpose of this study was to investigate whether
there was significant differential activation of the patient's
brain in response to hearing his mother's voice compared
with the voices of unknown women.

From the Institute of Neurology and Neurosurgery, Cuba (C. Machado, M


A Alvarez, L. Portela, M. Garcia, M Chinchilla, Y. Machado, Y Machado),
Department of Neurology, New York University Medical Center, New York.
USA (J Korein), Neuroscience Cuban Center (E. Aubert, J Bosch, P
Valdes), and the International Center for Neurological Restoration. Cuba (R
Rodriguez, N Perez).
Address requests for reprints to Calixto Machado, MD, PhD. Institute of
Neurology and Neurosurgery, Apartado Postal 4268, Ctudad de La Habana
10400. Cuba.
Ernail: braind@inforned sld cu
Received April 4, 2007, accepted April 11, 2007.

124
Downloaded from eeg.sagepub.com at Universidad Nacional Aut Mexic on March 15, 2015

02007 VOL. 38 NO. 3

CLINICAL EEG and NEUROSCIENCE

The power spectra of the EEGs recorded for the basal


record, listening to his mother's voice, and listening to 5
unknown women were averaged to obtain a grand average
spectrum for each electrode and for each experimental
condition. These grand averages were used for the subsequent analyses.
A Student's t-test was applied to assess significant differences for the EEG spectra between: "mother talks" vs.
"basal," "unknown women talk" vs. "basal." The statistical
significance threshold was corrected for Type I errors by
using the multiplicity factor introduced by Worsely et al,
based on the random field theory.14

RESULTS
In Figure l a mother talks vs. basal conditions are compared (red curve). Significant differences were found for
EEG frequencies from 14 to 58 Hz, with a peak at 33.2 Hz
(gamma band). No significant differences were found
between unknown women vs. basal conditions (black
curve). QEEGt maps, in the axial plane (Figure 1b), and in
a 3D reconstruction (Figure lc), showed that these statistical differences were localized in the lateral and posterior
regions of the left hemisphere.
DISCUSSION
Purhonen et all5 demonstrated that infants use more
attentional resources identifying the mother's voice than
unfamiliar ones, whereas Maddock et a116 found that emotional words activated posterior cingulate cortex bilaterally,
and that these regions may mediate interaction between
emotional and memory related processes. In the neonatal
period (birth to 28 days), an infant can already distinguish its
mother's voice from that of other women. These behavioral
features indicate a level of consciousness integration.1T-21
Di et a122 have recently evaluated the differences in
brain activation using fMRl in response to presentation of
the patient's own name spoken by a familiar voice in
patients with VS and MCS. These authors found significant
activation in primary auditory cortex in five of seven
patients with VS emphasizing the "classic pattern" of disconnected primary sensory cortex activation in patients
with VS. Nonetheless, they were surprised with the finding
of an atypical activation not only at the primary auditory
cortex, but also in hierarchically higher order associative
temporal areas in two VS cases. This activation pattern
was also observed in all 4 patients with MCS. The activated areas included the right posterior of the superior temporal sulcus. These 2 VS patients recovered to an MCS,
while the other 4 patients remained in VS.
Owen et a123.24 found residual cognitive functions indicating awareness in a persistent vegetative state patient
(PVS) by MRI, even though all clinical diagnostic criteria of
the VS were documented. They also noted that the comparison of speech with noise bursts revealed a significant
increase of the rCBF on the superior part of the temporal
plane bilaterally, and posterior to the auditory cortex in the

Figure 1.

a. Comparison of mother talks vs. basal record (red curve)


showed significant differences in the EEG spectrum for frequencies from 14 to 56 Hz. with a peak at 32.2Hz.No significant differences were found between unknown women vs. basal conditions (black curve).Axial QEEGt (Figure lb). and 3D maps

(Figure lc), illustrate localization of activation in the left lateral


and posterior region of the left hemisphere.
tors. Anatomical constraints were incorporated by using the
patient's individual MRI. The MRI image was segmented to
restrict the EEG sources to the gray matter within a grid of
3564 voxels. This technique is described elsewhere.9,11-'3
QEEGt was calculated in three experimental conditions
lasting 5 minutes, at weekly intervals: basal record (no
stimulus), listening to his mother's voice, and listening to 5
unknown women the same age as the mother who repeated the same words as the mother. We used maternal
expressions commonly used in the patient's daily life.
Translated from Spanish to English the questions were:
"My baby, mother is here, do you want to play with your
doggy? He is here beside you." The study was conducted
in the patient's room at home.
125

Downloaded from eeg.sagepub.com at Universidad Nacional Aut Mexic on March 15, 2015

02007 VOL. 38 NO. 3

CLINICAL EEG and NEUROSCIENCE

special imaging facilities, whereas QEEGt data, like those


used in this study, can be obtained at the bedside with conventional instrurnentation.10
Hence, the main result of this paper is that our 8-yearold PVS patient showed a broad activation of the EEG
power spectrum when his mother talked to him, meanwhile
no significant differences were found when unknown
women spoke to him.
These results demonstrate recognition of the mother's
voice and indicate high-level residual linguistic processing
in a patient meeting clinical criteria for VS. These findings
launch new ethical and practical implications for the management of VS patients.

region of the planum temporale, in the left hemisphere


only. They concluded that the observations provided compelling evidence for high-level residual linguistic processing in a patient with VS, and that some of the processes
involved in activating, selecting and integrating contextually appropriate word meanings may be intact in the PVS.
Nonetheless, for interpreting our resuits it is necessary
to consider the time and space resolutions in assessing
brain function comparing neurophysiologic with other neuroimaging methods. QEEGt directly reflects immediate
neuronal activation, because this technique entails a high
time resolution. Measurements made with fMRI, PET or
SPECT are not only more indirect but require transport to

REFERENCES
1 Machado C. The minimally conscious state. definition and
diagnostic criteria. Neurology 2002; 59: 1473-1474.

13. John ER, Prichep LS, Kox W, et al. Invariant reversible QEEG
effects of anesthetics. Conscious Cogn 2001; 10: 165-183.

2 Machado C. Cerebral processing in the minimally conscious


state. Neurology 2005, 65: 973-974.

14. Worsely KJ, Taylor JE, Tomaiuolo F, Lerch J. Unified univariate and multivariate random field theory. Neuroimage 2004;
23 (SUPPI1): S189-SI95.

3 Machado C. Can vegetative state patients retain cortical processing? Clin Neurophysiol 2005, 116: 2253-2254.

15. Purhonen M, Kilpelainen-Lees R, Valkonen-Korhonen M,


Karhu J, Lehtonen J. Cerebral processing of mother's voice
compared to unfamiliar voice in 4-month-old infants. Int J

4 Machado C. Terminating artificial nutrition and hydration in


persistent vegetative state patients: current and proposed
state laws Neurology 2007; 68: 312-313.

PsychOphysiol2004; 52: 257-266.


16. Maddock RJ, Garrett AS, Buonocore MH. Posterior cingulate
cortex activation by emotional words: fMRI evidence from a
valence decision task. Hum Brain Mapp 2003; 18: 30-41

5 Fins JJ, Schiff ND, Foley KM. Late recovery from the minimally conscious state: ethical and policy implications.
Neurology 2007; 68 304-307.

17. Korein J. Ontogenesis of the fetal nervous system: the onset


of brain life. Transplant Proc 1990; 22: 982-983.

6 Giacino JT, Hirsch J. Schiff N. Laureys S. Functional neuroimaging applications for assessment and rehabilitation
planning in patients with disorders of consciousness. Arch
Phys Med Rehabil2006; 87: S67-S76

18. Korein J. Reality and the brain: the beginnings and endings
of the human being. Brochman J, (ed). The Reality Club.
New York: lynx Books; 1988: 71-105.

7 Laureys S, Giacino JT, Schiff ND, Schabus M, Owen AM.


How should functional imaging of patients with disorders of
consciousness contribute to their clinical rehabilitation
needs? Curr Opin Neurol 2006; 19: 520-527.

19. DeCasper AJ, Spence MJ. Prenatal maternal speech influences newborn perception of speech sounds. Infant Behav
Develop 1986, 9: 133-150.

8 Giacino JT. Kalmar K. Diagnostic and prognostic guidelines


for the vegetative and minimally conscious states.
Neuropsychol Rehabil 2005; 15: 166-174.

20. DeCasper AJ, Maugais R, lecanuet JP, Granier-Deferre C,


Busnel MC. Familiar and unfamiliar speech elicit different
cardiac responses in human fetuses. Presented lntl SOC
Develop Psychol. Annapolis, MD; 1986.

9 Bosch-Bayard J, Valdes-Sosa P, Virues-Alba T, et al. 3D statistical parametric mapping of EEG source spectra by means
of variable resolution electromagnetic tomography (VARETA). Clin Electroencephalogr 2001; 32: 47-61.

21

DeCasper AJ. Fifer WP. Of human bonding newborns prefer


their mothers' voices. Science 1980; 208: 1174-1176.

10 Machado C, Cuspineda E, Valdes P, et al. Assessing acute


middle cerebral artery ischemic stroke by quantitative electric
tomography. Clin EEG Neurosci 2004; 35: 116-124.

22. Di HB, Yu SM, Weng XC, et al. Cerebral response to patient's


own name in the vegetative and minimally conscious states.
Neurology 2007; 68: 895-899.

11 Prichep LS, John ER. Tom ML. Localization of deep white


matter lymphoma using VARETA: a case study. Clin Electroencephalogr 2001; 32: 62-66

23

12 Johnston B, Seshia SS Prediction of outcome in non-traumatic coma in childhood. Acta Neurol Scand 1984, 69'
41 7-427.

24. Owen AM, Coleman MR, Boly M. Davis MH, Laureys S,


Pickard JD. Detecting awareness in the vegetative state.
Science 2006; 313: 1402.

Owen AM, Menon DK, Johnsrude IS, et al. Detecting residual


cognitive function in persistent vegetative state. Neurocase
2002; 8 : 394-403.

126
Downloaded from eeg.sagepub.com at Universidad Nacional Aut Mexic on March 15, 2015

You might also like