The Visual Word Form Area remains in the dominant hemisphere for language in late-onset left occipital lobe epilepsies: A postsurgery analysis of two cases
Introduction
A significant effort has been dedicated to understanding the neurobiological basis of word recognition (reviewed by Wandell [1] and Dehaene [2]), a fundamental basis for reading. An important concept that has emerged is the Visual Word Form Area (VWFA), which was first proposed by Cohen [3] as a specialized cortical localization able to perform automatic word recognition from letter strings. A variety of sources of information ranging from lesion analysis [4], [5], cortical stimulation [6], functional magnetic resonance imaging (fMRI) [7], [8], and evoked potentials [9], [10] to outcome of surgery for epilepsy [11] converge on the demonstration of a consistent localization for the VWFA in the middle fusiform gyrus of the left hemisphere [12]. In testing with fMRI, several contrasts are effective in activating the VWFA, ranging from the contrast between words and phase-scrambled words [13]; familiar and unfamiliar characters [14]; and letter strings, words, and checkboards [15], [16] as well as false fonts; frequent and infrequent letters; and real words [17]. A bilateral ventral occipitotemporal activation is expected to be observed mostly in the left hemisphere. This asymmetric activation is expected when using verbal stimuli presented in the middle of the vision field [13], [17].
This strong anatomical–functional relationship has important consequences for surgery for occipital and temporal lobe epilepsies, which place the patient at risk for development of postsurgical alexia [11]. This type of language impairment adds to the well-known risk of left side anterior fusiform gyrus resections [18], [19].
Several studies have demonstrated a strong correlation between the hemispheric localization of the VWFA and the lateralization of language in healthy subjects [9], [20], suggesting that the late specialization of the VWFA at the time of reading acquisition occurs in close relationship with the development of language networks in the same hemisphere. There are some data suggesting that despite left-hemisphere dominance for language, the specialization of the VWFA can localize to the right hemisphere when the original left side localization suffered a lesion in early childhood [21]. There are no data, however, about the effect of an epileptic focus developing in the neighborhood of the VWFA after reading acquisition. This piece of information would be of importance to assess the surgical risk of alexia. In view of the irreversible effect of late VWFA lesions [10], this is of obvious medical relevance.
Another important point concerning the organization of reading is whether the VWFA requires a functional connection with the neighbor secondary visual areas or is autonomous from them, a question that cannot be fully answered by correlational methods such as fMRI but that is well suited to lesional analysis. Nevertheless, an extended portion of the ventral occipitotemporal region is recruited in reading; Jobard [12] suggested that within the VWFA, there is a spatial hierarchal organization, with the most anterior part the one mostly recruited to process real words, but a potential disconnection within the VWFA and subsequent impairment in this “hierarchal organization” was not discussed. Important white matter bundles connecting these areas are the inferior longitudinal fasciculus (ILF) on the left [22] and a transcallosal bundle from the right hemisphere [23]. Interruption of one of these projection pathways has been postulated to lead to alexia limited to the contralateral visual hemifield [24].
We report on two patients who underwent to surgery for epilepsy arising in the inferior occipital cortex, in the immediate neighborhood of the VWFA, partially disconnecting this region from adjacent secondary visual areas. From the analysis of reading capabilities before and after surgery and comparison with similar cases from the literature, we draw conclusions regarding surgical decisions and the preservation of reading in late-onset occipital lobe epilepsies.
Section snippets
Patient 1
He is a right-handed 15-year-old boy, who had a normal development and was healthy until the age of 7 years, at which time he developed epilepsy with daily complex partial seizures, which proved refractory to medical therapy. The EEGs revealed a normal background with a very active spike focus on the left occipital–temporal area. The MRIs failed to demonstrate any structural lesion. The neurological examination was normal, including the confrontation visual fields.
With the onset of epilepsy,
Patient 1
Before surgery, he was an excellent student (second in his class), and the WISC-III was reported as normal but unavailable to us.
He underwent epilepsy surgery at the age of 9 years, with 4-day intracranial recording using subdural grids. During invasive monitoring, left dominance language mapping through subdural electrode stimulation was performed. During surgery, removal of a cortical inferior left occipital lobe area with continuous spike–wave discharges on ECoG recording was made (Fig. 1a,
Discussion
Our two patients submitted to left inferior occipital resections just posterior to the VWFA maintained their reading ability, demonstrating the capability of the VWFA to automatically process words even when partially disconnected from the neighbor secondary visual areas. More generally, this suggests that the functional integrity of the left-hemisphere visual ventral stream is not necessary for preserving the automatic processing of words, as long as the VWFA itself is preserved, although
Acknowledgments
The authors are grateful to Constança Jordão and Cristina Menezes for their technical support in the imaging and to Luis Ferraz for collaboration in language assessment.
Ricardo Lopes has been supported by the grant SFR/BD/65617/2009 from the Portuguese Foundation for Science and Technology (FCT). Rita Nunes has been supported by the FCT Investigator Program.
Conflict of interest
The authors have no conflicts of interest.
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