Elsevier

Brain and Language

Volume 142, March 2015, Pages 54-64
Brain and Language

Morphological derivation overflow as a result of disruption of the left frontal aslant white matter tract

https://doi.org/10.1016/j.bandl.2015.01.005Get rights and content

Highlights

  • We report a single case study on language production evaluated using electrical stimulation.

  • Intraoperative verb generation resulted in a morphological derivation overflow.

  • This disturbance appeared once the tumor resection reached the left frontal aslant tract (FAT).

  • Pre and post-surgical DTI confirmed the localization of the damage at the level of the FAT.

  • We are the first to propose a link between this tract and morphological processing.

Abstract

The frontal aslant tract (FAT) is a recently described major connection between the preSMA and Broca’s area, whose functional role remains undefined. In this study we examined a patient presenting a morphological overregularization strategy in a verb generation task during awake surgery. This specific language deficit coincided with brain tumor resection at the level of the left FAT. During the task execution the patient formed the non-existent verbs by applying a morphological derivation rule to the given nouns, instead of retrieving the appropriate verbs. DTI results confirmed left FAT damage. Neuropsychological follow-up showed that this morphological derivation impairment partially persisted after surgery, whereas the results on a wide spectrum of other language-related tasks remained satisfactory. Additionally, we compared the pre- and the post-operational fMRI activation maps for the same verb generation task. We discuss the potential role of the left FAT in the morphological derivation process and in lexical retrieval.

Introduction

The frontal aslant white-matter tract (FAT) has recently been described in detail using diffusion tensor imaging (DTI) in humans (Catani et al., 2012, Ford et al., 2010, Lawes et al., 2008, Oishi et al., 2008) and monkeys (Thiebaut de Schotten, Dell’Acqua, Valabregue, & Catani, 2012) but is one of the fasciculi whose functional role continues to be unresolved. The FAT is formed by the white-matter fiber bundles descending from the anterior cingulate cortex and the pre-supplementary motor area (preSMA) to Broca’s area (pars opercularis of the inferior frontal gyrus, BA 44). Considering its anatomical relation to these gray matter areas, it was hypothesized that this tract could be part of an extended network involved in initiating and coordinating complex eye, head and arm movements in reaching actions (Catani et al., 2012). In line with this proposal that the FAT is involved in specific motor functions, a recent ESM-case study by Martino and colleagues (Martino, de Lucas, Ibáñez-Plágaro, Valle-Folgueral, & Vázquez-Barquero, 2012) revealed that electrical stimulation of the right FAT caused Foix-Chavany-Marie syndrome, a rare type of suprabulbar palsy affecting the orofacial musculature.

When we consider the possible functional role of the FAT in language processing it is the left hemisphere that should draw our focus. The main reason that suggests an important role of this white-matter pathway in language processing is the anatomical connectivity with regions involved in controlled lexical retrieval, syntactic processing, language production and monitoring.

Broca’s area is known to be crucial for word production (Grodzinsky & Santi, 2008), controlled lexical retrieval (Novick et al., 2005, Schnur et al., 2009, Thompson-Schill et al., 1997), grammatical and morphological processing (Bozic et al., 2013, Bozic et al., 2010, Shapiro and Caramazza, 2003), whereas the SMA is related to speech initiation, coordination, performance and speech monitoring (Alario et al., 2006, Chauvel et al., 1996, Crosson et al., 2001, Fried et al., 1991, Gabarrós et al., 2011, Indefrey, 2011, Indefrey and Levelt, 2004, Krainik et al., 2003, Laplane et al., 1977, Pai, 1999). Therefore, more posterior connections with SMA are related to motor aspects of articulation. Loss of integrity of the left FAT is associated with a decline in verbal fluency (Catani et al., 2013, Kinoshita et al., 2014, Mandelli et al., 2014), and its electrical intraoperative stimulation results in disturbance of speech initiation (Kinoshita et al., 2014). In contrast, connections to preSMA are more related to linguistic processing (Catani et al., 2013). In a handful of studies (Alexander et al., 1987, Hogan et al., 2006, Naeser et al., 1989) it has been reported that patients suffering from deep lesions in the periventricular white matter of the frontal lobe presented impaired fluency, agrammatism (i.e., impaired syntactic processing) and reduced performance monitoring, which could be explained by a disconnection of the frontal aslant and fronto-striatal tracts. Finally, more anterior connections to medial prefrontal cortex are likely to be involved in social cognition and theory of mind (Catani & Bambini, 2014). Moreover, this tract is left lateralized in right-handed subjects (Catani et al., 2012) which gives further weight to its possible role in language processing.

In our study we mainly focused on derivational morphology – one of the most important mechanisms of word formation based on the combination between word stems (e.g. happy, speak) and derivational morphemes (e.g. -un, -ness, -er in English). This mechanism may be used to form words from both the same (e.g. happy, unhappy-adjectives) and distinct grammatical categories (e.g. happy, happiness-adjective to noun; speak-speaker-verb to noun) in contrast to inflection, the product of which always represents the same grammatical category (e.g. speak, speaks, speaking, spoken-verb); (Bozic et al., 2010, Marangolo et al., 2003). In the present work, we used distinct tasks to study derivation and inflection. We used noun-based verb generation and verb-based noun generation tasks to assess derivational morphology and we used the morphological transformation task to evaluate inflection (see Table 1).

Importantly, derivational patterns differ in their level of productivity with some being more commonly used for word formation than others. We investigated a case of a patient who presented an unusual strategy of overregularization, applying a very frequent Spanish morphological derivation rule. This rule is highly productive serving to generate verbs from nouns by attaching the suffix –ear to the noun to create an infinitive verb (e.g., from the loan word “chat”, the derived verb is created by attaching the suffix –ear to the stem, “chatear”). In a noun-based verb generation task we clearly observed a strong tendency for the patient to apply this particular rule and create new non-existing verbs in Spanish (e.g., from the noun “libro” – meaning book, the verb “librear” was created instead of retrieving the correct associated verb “leer”, to read). Given that this phenomenon occurred during the removal of a tumor at the level of the left FAT, we hypothesized that the disruption of this white-matter pathway affected the communication between cortical regions used to correctly retrieve the verbs associated to a specific noun however preserving the morphological derivation processes involved in creating new verb forms. Electrical Stimulation Mapping (ESM) combined with refined neuropsychological testing allowed us to control the noun-based verb generation task performance during surgery.

Even if speech disturbances were previously observed during the course of intraoperative stimulation of the left FAT (Kinoshita, 2014), to our knowledge, this is a first report showing word retrieval deficits in a noun–verb morphological derivation task related to the intraoperative stimulation of this tract.

Section snippets

Participant

The patient is a 39-year old right-handed Spanish monolingual woman, who underwent an asleep–awake–asleep brain surgery for tumor removal. According to the histological analysis, she harbored an anaplastic aligogastrocytoma (grade III WHO) with neither necrosis nor miscrovascular proliferation. This lesion was localized in the left premotor-frontal area encompassing Brodmann areas (BA) 6 and 8 (middle and superior frontal gyri) and indirectly affecting BA 9. Pre-surgery clinical fMRI

Electrical stimulation mapping

The exact localization of the ESM points on the cortical level was reproduced based on intraoperative photographs. An arbitrary, two-dimensional grid was placed on the picture and the exact localization of points was transferred to a patient’s 3D cortex reconstruction. The ESM cortical mapping revealed that the stimulation of the motor cortex induced involuntary movements and the stimulation of the premotor cortex altered the alternate hands movement (in this motor task the patient continuously

Discussion

This case study examines a 39 year-old woman who underwent the asleep–awake–asleep brain surgery for left premotor-frontal tumor removal. When presented with a noun-based verb-generation task during the surgery, the patient failed to correctly generate verbs from nouns, repetitively using an overregularization strategy: in order to produce a verb, she was attaching a very productive suffix in Spanish morphological derivation –ear to the noun stem. This observation coincided with the stimulation

Acknowledgments

The authors would like to acknowledge Estela Càmara, Diana López-Barroso and Pablo Ripollés for their help in the DTI data analysis and also Matti Laine and Michael Ullman for their constructive remarks on the interpretation of the results. This project has been supported by the Catalan Government (2009 SGR 93) and the Spanish Government (MICINN, PSI2011-29219) awarded to ARF and a pre-doctoral FPU Spanish Government grant to JS.

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