American Journal of Neuroradiology 24:42-44, January 2003
© 2003 American Society of Neuroradiology
Case Report
PEDIATRICS
Language Processing during Natural Sleep in a 6-Year-Old Boy, as Assessed with Functional MR Imaging
Marko Wilkea,b,
Scott K. Hollanda and
William S. Ball, Jra
a Imaging Research Center, Cincinnati Children’s Hospital Medical Center, OH
b Department of Psychiatry, Cincinnati Children’s Hospital Medical Center, OH
Address reprint requests to Marko Wilke, Imaging Research Center, Cincinnati Children’s Hospital Medical Center (ML 5031), 3333 Burnet Avenue, Cincinnati, OH 45229
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Abstract
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Summary: Functional MR imaging for language lateralization was
performed in a 6-year-old child before neurosurgical intervention.
A passive story-listening task was used; this revealed a bilateral
language network. The task was repeated during the same session
when the child had fallen asleep and surprisingly yielded strong
activation in similar language areas. Our findings suggest that
language processing does occur during natural sleep, even in
young children. This potentially allows for an assessment of
language functions, even in sleeping children.
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Introduction
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Although functional MR imaging has been used with success in
young children, it has been limited by their ability to cooperate
in the awake state. Earlier studies have demonstrated limited
success in studying sensory activation in the sedated child
(
1,
2) but not during natural sleep. In fact, surprisingly little
is known about the brain’s physiology during sleep and,
indeed, about the very purpose of sleep itself. The extent to
which brain processes during sleep differ from those during
the awake state remains unclear. The recent application of functional
imaging methods has renewed research interest in this field
(
3).
We report on a young boy who was referred for functional MR imaging as part of presurgical planning to assess language lateralization. The same language task was conducted while the patient was awake and while he was asleep, with surprising results. The results of this case are compared with data from four healthy 6-year-old boys performing the same task.
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Case Report
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A 6-year-old right-handed boy was seen by a neurologist for
complex partial seizures. MR imaging was performed and demonstrated
an enhancing left mesial temporal lobe lesion (
Fig 1), which,
after resection, was confirmed to be a ganglioglioma. As part
of the presurgical evaluation, the child was scheduled for a
functional MR study to evaluate the proximity of language function
to the left temporal lobe lesion. Internal review board approval
and informed consent were obtained before imaging was performed.
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FIG 1. Contrast-enhanced T1-weighted image demonstrates the enchancing lesion in a 6-year-old boy with complex partial seizures in the left temporal lobe.
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Imaging was performed with a Biospec 30/60 3-T MR imager equipped with a head gradient insert (Bruker SK330; Bruker Medizintechnik, Ettlingen, Germany). Functional images were acquired by using a gradient-echo T2*-weighted echo-planar sequence (TR/TE, 3000/38; in-plane resolution, 4 x 4 mm; section thickness, 5 mm), yielding 24 sections over 110 time points during the alternating 30-second periods of control and activation. The total imaging time was 5 minutes 30 seconds. A T1-weighted, three-dimensional whole-brain image was also acquired (15/4.3, 1 x 1.5 x 2.25 mm). Postprocessing was performed by using Cincinnati Children’s Hospital Image Processing Software (CCHIPS) and included the removal of Nyquist ghosts and geometric distortions by use of a multiecho reference image (4). Motion correction was accomplished by using C routines. Images were analyzed using a cross-correlation technique.
Because of the age of the child, a passive-listening task (stories vs tones) was performed. Although the child was able to complete the functional task, the motion of his hands and arms during the study impaired the quality of the image. Motion, which reduces the correspondence between images acquired at different points in time, generally degrades the ability to correctly detect functional activation, because it interferes with the ascription of substantial signal intensity changes to a given voxel. To give the child time to settle down, an anatomic image was acquired. When the boy was approached to explain the next task, it was found that he had fallen asleep. It was decided to repeat the study, and he was still asleep when he was removed from the imager bore several minutes later.
Although the image obtained when the patient was awake revealed limited activation in both the Broca and Wernicke areas in the left cerebral hemisphere (Fig 2B, top row), activation was not only present in similar language areas on the sleep image but also far more brisk (Fig 2B, bottom row).
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FIG 2. Functional MR data obtained in subjects who were performing a story-listening task.
A, Reference data from four healthy 6-year-old boys obtained while they were listening to stories (active condition) or tones (control condition). Note the variability in the activation patterns.
B, Imaging data from our patient who performed the same task while awake (top) and in the sleeping state (bottom). Cross-correlation r=0.375, cluster size=5. Note that, at the same analysis threshold, stronger activation is shown in the sleep study
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Discussion
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The visualization of eloquent cortical regions near a brain
lesion has gained widespread attention, because this information
may aid in minimizing postoperative neurologic deficits. Functional
MR imaging allows for the noninvasive detection of differences
in blood flow that are associated with neuronal activation,
with high temporal and spatial resolution. We report the case
of a 6-year-old boy who underwent clinical functional MR imaging
for presurgical planning of language lateralization because
of a temporal-lobe lesion (
Fig 1). The purpose of the study
was to assess a possible interference with language-related
areas with the surgical approach. The same listening-to-stories
task was performed with the patient awake and after he had fallen
asleep. The study revealed strong activation in similar language
areas, indicating language processing during natural sleep.
The detected pattern of bilateral activation (as assessed by
calculating a weighted laterality index [
5]) is in accordance
with the high degree of variability in this age group (
Fig 2).
Both images reveal remarkably similar patterns of neuronal activation, indicating that the receptive processing of heard speech does not differ fundamentally between the awake and sleeping states in this child. Similar results were seen in a combined EEG–functional MR study in adults, in which, as in our subject, only the language component of a passive listening task activated language-related brain areas (6). This case is interesting, because the child performed the same (passive) task while awake and during natural sleep; this procedure allowed us to rule out the effects of sedative agents. Although functional MR imaging has been conducted in young children under sedation (1), sedative agents have been shown to have a notable effect on the blood oxygen level–dependent (BOLD) response (7); this finding limits the conclusions to be drawn from such studies (2). Despite this advantage, however, the comparability of the two studies conducted in this child is still hampered by the involuntary motion on the first image that was not present on the second image.
Because this finding was a chance observation, no EEG recordings were available to assess the sleep stages. However, the child was asleep immediately before and after the image acquisition, and actually, he did not wake up until he was taken out of the imager several minutes after the completion of this study. Interestingly, when the pixel intensity–time courses of receptive and expressive language areas (traditionally known as the Wernicke and Broca areas [8]) are analyzed, they seem to differ substantially, with only the receptive language areas displaying a constant and robust correlation with the reference function (Fig 3). Activation in expressive areas shows a more fluctuating course and becomes robust only in the second half of the 5
-minute imaging session, whereas receptive brain areas show almost no fluctuation. This effect can be speculated to reflect different sleep stages, which is in accordance with a recent observation of a notable effect of the sleep stage on the magnitude of the BOLD response (9). In addition to a global influence, our data suggest a differential effect of different sleep stages on these areas that could be due to either anatomic or functional differences. Continuous EEG recordings would have been necessary to verify this effect.
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FIG 3. Functional MR data obtained while patient was asleep.
A, Activation patterns observed during the sleeping study show activation in the expressive (top) and receptive (bottom) language areas.
B, Pixel intensity and time courses correlated with the reference function. Note the difference in responses between the expressive (top) and receptive (bottom) areas during the first three blocks. This finding suggests a regionally different response to the auditory stimulus.
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Conclusion
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Our observations have two major implications: First, they demonstrate
that language processing during sleep is not an exclusive function
of the mature brain but that it can already be detected in young
children in whom language functions are still developing (
5).
Our findings also suggest differing effects of sleep stages
on distinct brain areas. Second, by showing that language processing
does occur during natural sleep, these observations indicate
that this central higher brain function is amenable to functional
imaging studies, even in young children in the sleep state.
If natural sleep can be achieved, the confounding effects of
sedative agents can thus be avoided, and robust motion-free
cortical activation can still be achieved.
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Acknowledgments
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We would like to thank John S. Myseros, MD, and Douglas F. Rose,
MD, for referring their patient.
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Received June 18, 2002;
accepted after revision July 12, 2002.
TOP
Abstract
Introduction