Interindividual uniformity and variety of the “Writing center”: A functional MRI study
Introduction
Writing is one of the most important tools of communication and is a uniquely human skill. Much of our knowledge of the functional neuroanatomy associated with writing has been derived from lesion studies, especially studies of pure agraphia. Pure agraphia, i.e., impairment of the ability to write in the absence of abnormalities in other language modalities, can be caused by a lesion in the following regions: the posterior part of the left middle frontal gyrus (MFG), namely, Exner's area (Exner, 1881, Anderson et al., 1990, Tohgi et al., 1995); the left intraparietal sulcus (IPS) (Kinsbourne and Rosenfield, 1974, Basso et al., 1978, Auerbach and Alexander, 1981, Takayama et al., 1994). Recently, some functional magnetic resonance imaging (fMRI) studies have attempted to reveal the brain areas related to writing in normal subjects (Sugishita et al., 1996, Nakamura et al., 2000, Katanoda et al., 2001, Menon and Desmond, 2001, Beeson et al., 2003). The results of most of these studies have suggested that the brain regions crucial to writing are the left MFG and the left IPS, whereas other sites of brain areas have also been suggested to be related to writing, e.g., the right IPS, the region(s) surrounding either or both of the left and right cingulate sulci (Sugishita et al., 1996), the supplementary motor cortex (Menon and Desmond, 2001), and the left posterior inferior temporal cortex (PITC) (Nakamura et al., 2000, Beeson et al., 2003). However, no unequivocal results have been reported to date.
Although rare, left-hand agraphia also has provided a unique opportunity to consider the functional neuroanatomy associated with writing. Left-hand agraphia is known as a symptom due to callosal disconnection syndrome (Liepmann and Maas, 1907), and this disorder is considered to be caused by lesions in the posterior corpus callosum (Sugishita et al., 1980, Gersh and Damasio, 1981). Observations of patients with left-hand agraphia suggest that left-hand writing is performed in cooperation between the right and left cerebral hemispheres. However, little is known about the neuroanatomy involved in left-hand writing. An investigation of the cerebral mechanism of left-hand writing may provide the clue to reveal the neural substrates of writing.
The aim of the present fMRI study was to elucidate the neural substrates of writing using novel paradigms including writing with right and left hands tasks. To the best of our knowledge, this is the first functional imaging study of writing using a left-hand writing task. We employed Japanese phonograms (Kana), in which each phoneme is represented by only a single grapheme (Kana), so that phoneme–grapheme conversion is extremely simple. In English, on the other hand, most phonemes are represented by two or more graphemes; accordingly, phoneme–grapheme conversion is complex (Sugishita et al., 1999). We also used a conjunction method in fMRI (Price and Friston, 1997, Friston et al., 1999, Friston et al., 2005, Nichols et al., 2005). Here, common areas of activation were identified while subjects performed writing tasks with the right hand or the left hand. Our hypothesis is that the areas of activation obtained in this type of conjunction analysis would be crucial to the central process of writing, as these areas are not expected to be activated as a result of finger movements used to reproduce letters.
Section snippets
Subjects
Twenty healthy volunteers (15 males and 5 females, age 18–29, mean = 23.0, standard deviation (SD) = 4.3) were recruited by word of mouth in the community in Tokyo, Japan. All subjects were native Japanese speakers with a university education. The Edinburgh Handedness Inventory laterality quotients (Oldfield, 1971) ranged from 70 to 100 (mean = 93.2, SD = 9.8), indicating a strong right-hand preference for all subjects. Informed consent was obtained from each subject prior to the experiment.
Tasks and stimuli
Right-hand writing (WR) > Rest (RE)
The results of the WR > RE contrast are shown in Fig. 2A. A large activation was observed in the left frontoparietal cortical region, i.e., the posterior end of the left superior frontal gyrus (SFG) extending to the left superior parietal lobule (SPL). Activations were also observed in the following areas: the bilateral occipital cortex extending to the bilateral lingual and fusiform gyri, and to the left posterior inferior temporal gyrus; the bilateral inferior parts of the precentral gyri;
Discussion
We examined brain activation during three experimental conditions: WR (written naming with the right hand), WL (written naming with the left hand), and NA (silent naming). Our primary analysis was conducted in order to investigate the conjunction of the WR > NA and WL > NA contrasts, and this analysis was expected to shed light on the brain mechanism involved in the central process of writing (Fig. 1). The group analysis revealed significant activation in the following three areas of the brain:
Conclusion
The current study revealed the following three areas are crucial to the central process of writing: (1) the posterior end of the left superior frontal gyrus, (2) the anterior part of the left superior parietal lobule, and (3) the lower part of the anterior limb of the left supramarginal gyrus. Whereas the first two of the above three areas were found to be crucial for writing in all individuals, an interindividual inconsistency of involvement with writing was observed in three areas: the lower
Acknowledgments
This study was supported by a grant (L-2-12) from the Japan Society for the Promotion of Sciences. The authors thank Dr. Kohki Yoshikawa for his cooperation and helpful advice.
References (58)
- et al.
Lesion localization of phonological agraphia
Brain Lang.
(1992) - et al.
Acquired agraphia caused by focal brain damage
Acta Psychol.
(1993) - et al.
Cognitive conjunction and cognitive functions
NeuroImage
(2004) - et al.
The Talairach coordinate of a point in the MNI space: how to interpret it
NeuroImage
(2005) - et al.
Distinct unimodal and multimodal regions for word processing in the left temporal cortex
NeuroImage
(2004) - et al.
Multisubject fMRI studies and conjunction analyses
NeuroImage
(1999) - et al.
Conjunction revisited
NeuroImage
(2005) - et al.
Functional lateralization of the human premotor cortex during sequential movements
Brain Cogn.
(2002) - et al.
Anatomical variability of the lateral frontal lobe surface: implication for intersubject variability in language neuroimaging
NeuroImage
(2005) - et al.
Agraphia selective for written spelling: an experimental case study
Brain Lang.
(1974)