ERM 0205 INSERM-CEA, Service Hospitalier Frédéric Joliot, Orsay, and Service de Radiologie Pédiatrique, Hôpital Necker Enfants Malades, Paris
INSERM Unité 316, CHU Bretonneau, Tours
ERM 0205 INSERM-CEA, Service Hospitalier Frédéric Joliot, Orsay
Service des Urgences Cerebro-Vasculaires, Groupe Hospitalier Pitié-Salpêtrière, Paris
ERM 0205 INSERM-CEA, Service Hospitalier Frédéric Joliot, Orsay, and Service de Radiologie Pédiatrique, Hôpital Necker Enfants Malades, Paris
ERM 0205 INSERM-CEA, Service Hospitalier Frédéric Joliot, Orsay, France
Correspondence: Mônica Zilbovicius, Service Hospitalier Frédéric Joliot, DRM, DSV, CEA, 4 Place du General Leclerc 91406, Orsay, France. Tel: +33 (1)01 69 86 78 90; fax: +33 (1)01 69 86 77 28; e-mail: zilbo{at}shfj.cea.fr
Declaration of interest None. Funding detailed in Acknowledgements.
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ABSTRACT |
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Aims To map the exceptional calendar capacity of a man with primary autism.
Method Positron emissiontomography was used to map brain activity in a man who is able to associate a day of the week with the corresponding calendar date.
Results During the calendar task, the left hippocampus, the left frontal cortex and the left middle temporal lobe were activated.
Conclusions The cerebral circuit involved in this man's prodigious calendar skill is similar to that normally involved in memory retrieval tasks. These results suggest that the prodigious capacities may be sustained by memory processing.
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INTRODUCTION |
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To investigate the neural network implicated in prodigious calendar ability, we performed a positron emission tomography (PET) activation study in a 22-year-old savant with prodigious calendar capacities. Despite severe behavioural and cognitive impairment, he was able to generate, in a few seconds, a weekday corresponding to a date. He had been able to perform this association for the previous 18 years (since he was 4 years old) but was unable to perform this for future dates. Therefore we hypothesised that his prodigious calendar abilities were sustained by memory processing.
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METHOD |
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An ethics committee approved this study and examination was performed with the informed written consent of the parents.
Brain imaging protocol
Positron emission tomography (PET) uses positron-emitting labelled carriers
to produce an image of brain activity. One of the applications of PET is the
study of functional brain activity by measuring regional cerebral blood flow
during the performance of cognitive tasks. Regional changes in cerebral blood
flow between two tasks reflect the mobilisation of functional units specific
to the new task. Hence it is possible to identify the brain regions activated
by the stimulus. The purpose of this study was to identify the regions
activated by performance of the calendar task. To do this, blood flow images
were obtained at base-line and during performance of the task and the two
images were subtracted. Those regions that had been activated showed a change
in blood flow.
Task
In the calendar task dates were chosen randomly over a period of 16 years
(1982-1998). During the scan, dates were given orally by the investigator and
the young man was asked to answer orally the day of the week that corresponded
to the date (e.g. 26 February 1982 Friday). Fifteen dates were given during
100 s of PET acquisition (1 question/answer every 6 s).
In the word repetition control task a list of French objects was selected (e.g. car, house, toys). The investigator gave orally the name of an object and the young man was asked to repeat it orally (50 words during the 100 s of PET acquisition) in order to control for auditory perception and word production.
Image acquisition
Scanning was performed using an ECAT Exact HR+962 PET camera (Siemens,
Knoxville, Tennessee, USA). Attenuation-corrected data were reconstructed into
63 slices, with a resulting resolution of 5 mm full width at half maximum.
Relative cerebral blood flow was determined from the distribution of
radioactivity after bolus intravenous injections of H
152O (Fox et
al, 1984). Twenty seconds before each scan, 10 mCi of H
152O was administered by an intravenous bolus injection.
Data were collected over 80 s. The young man was lying in the scanner in a
quiet darkened room. Three measurements of relative cerebral blood flow were
performed: (1) at rest; (2) during the auditory calendar task; and (3) during
a control repetition of words. Tasks started 20 s before image acquisition.
Three-dimensional Three-dimensional T1 high-resolution MRI of the brain
(General Electric 1.5-T Signa system, GE Medical Systems, Milwaukee,
Wisconsin, USA) was also performed on the same day.
Image analysis
Statistical parametric mapping software (SPM96, Wellcome Department of
Cognitive Neurology, London) was used for image realignment, transformation
into standard stereotactic space
(Talairach & Tournoux,
1988), smoothing (15 mm Gaussian kernel) and statistical analysis
(Friston et al, 1995).
State-dependent differences in global flow were corrected using proportional
scaling. To assess the individual pattern of activation we designed a
multistudy model matrix. Images of five normal controls during rest were
included in the model, allowing an estimation of inter-participant
variability.
The three conditions (rest, calendar task and word repetition) were compared using the t-statistic subsequently transformed into a normally distributed Zstatistic. Z-maps were thresholded at 3.09 (P50.001).
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RESULTS |
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The word repetition task induced activation of the left frontal (BA 6, 9, 10, 44), left temporal (BA 21, 22, 39) and right precentral and postcentral frontal cortex (BA 6, 4 and 43) (Z-score 43.09, P50.001) compared with rest. There was no activation in the left hippocampus during the word repetition task.
Specific calendar task activation (calendar task compared with word repetition task, Fig. 1) was associated with significant activation (Z-score 43.09, P50.001) of the left hippocampus, of the left middle temporal gyrus (BA 21) and of the left inferior frontal gyrus (BA 47, 45).
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DISCUSSION |
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We performed a PET activation study to identify a brain network implicated in the prodigious calendar aptitude in people with autism. The present results show that the young man's capacity to associate a day of the week with a corresponding date of the calendar was associated with significant activation of a left fronto-temporal network, including the hippocampus, which is strongly implicated in memory processing (Cipolotti et al, 2001; Nadel & Moscovitch, 2001). This hippocampal activation is in agreement with the clinical hypothesis that the young man's prodigious calendar capacity was sustained by memory processing.
However, the present findings must be considered in the light of some methodological limitations. First, as the calendar day-date association task is unusual, we have not compared the pattern of brain activation with that of normal controls. A study with a large number of individuals with the same savant capacities and an appropriate control group would help to establish a more general mechanism for this capacity in autism.
Second, the choice of a control task for the calendar condition was complex. The word repetition task controls for some aspects of speech perception and production but not for all cognitive components of the calendar task. This choice could limit the interpretation of the pattern of activation observed during the calendar task. However, the hippocampal activation was observed when comparing the calendar task with both control and rest conditions, and was not detected during the word repetition task. This implicates the hippocampus in the present calendar task. However, we cannot generalise the findings in this single individual to savant abilities in populations.
Despite these methodological limitations, this preliminary study disclosed a cerebral circuit involved in the prodigious calendar capacity of a savant. The pattern of activation observed during the calendar task implicated a selective brain network including the left inferior frontal cortex, the middle temporal cortex and the hippocampus. This network is normally activated during delayed memory retrieval processing in normal controls (Dupont et al, 2001). Therefore, the present results suggest that the prodigious calendar capacity of this young man may be sustained by a special memory processing.
These findings may lead to speculation that during development people with autism can 'overdevelop' a normal brain circuit and develop prodigious capacity, despite their severe cognitive and behavioural handicaps. The prodigious calendar capacity in autism and its associated brain network should be regarded in the light of an early developmental disorder. Autism might be associated with a developmental disorganisation of the neural circuits, facilitating the emergence of these peculiar networks.
Finally, our study illustrates how functional brain imaging offers a new perspective for the investigation of brain mechanisms underlying the still mysterious autistic savant syndrome.
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Clinical Implications and Limitations |
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LIMITATIONS
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ACKNOWLEDGMENTS |
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Received for publication February 17, 2004. Revision received October 19, 2004. Accepted for publication October 21, 2004.