Elsevier

NeuroImage

Volume 47, Issue 2, 15 August 2009, Pages 700-704
NeuroImage

Dissociable neural representations of grammatical gender in Broca's area investigated by the combination of satiation and TMS

https://doi.org/10.1016/j.neuroimage.2009.04.097Get rights and content

Abstract

Along with meaning and form, words can be described on the basis of their grammatical properties. Grammatical gender is often used to investigate the latter as it is a grammatical property that is independent of meaning. The left inferior frontal gyrus (IFG) has been implicated in the encoding of grammatical gender, but its causal role in this process in neurologically normal observers has not been demonstrated. Here we combined verbal satiation with transcranial magnetic stimulation (TMS) to demonstrate that subpopulations of neurons within Broca's area respond preferentially to different classes of grammatical gender. Subjects were asked to classify Italian nouns into living and nonliving categories; half of these words were of masculine and the other half of feminine grammatical gender. Prior to each test block, a satiation paradigm (a phenomenon in which verbal repetition of a category name leads to a reduced access to that category) was used to modulate the initial state of the representations of either masculine or feminine noun categories. In the No TMS condition, subjects were slower in responding to exemplars to the satiated category relative to exemplars of the nonsatiated category, implying that the neural representations for different classes of grammatical gender are partly dissociable. The application of TMS over Broca's area removed the behavioral impact of verbal (grammatical) satiation, demonstrating the causal role of this region in the encoding of grammatical gender. These results show that the neural representations for different cases of a grammatical property within Broca's area are dissociable.

Introduction

Words are complex symbols encoding not only sound and meaning but also grammatical information such as gender. Although English doesn't use it, grammatical gender is a common property of many languages and plays a fundamental role in syntactic processing. Neuroimaging evidence suggests that several cortical regions contribute to syntactic processing (e.g., Damasio and Trannell, 1993, Warburton, 1996, Caplan, 2006), but Broca's area in the left inferior frontal cortex is perhaps most strongly associated with syntax because lesions to this area often result in grammatical deficits (Miceli et al., 1989, Vanier and Caplan, 1991, Shapiro and Caramazza, 2003, Caplan, 2006). Furthermore, Miceli et al. (2002) showed using functional magnetic resonance imaging (fMRI) that grammatical feature task activated areas of the left middle and inferior frontal gyrus and of the left middle and inferior temporal gyrus.

Only a few studies, however, have investigated the causal role of the left inferior frontal gyrus (IFG)/Broca's area in syntactic processing in neurologically normal observers. This can be accomplished by the use of transcranial magnetic stimulation (TMS), a noninvasive tool for modulating neural activity, which can be used to determine the causal role of the targeted region in a given cognitive process (e.g. Cowey, 2005, Walsh and Pascual-Leone, 2003, Devlin and Watkins, 2007). Previous TMS studies on Broca's area have either failed to find an effect on syntactic processing (Cappelletti et al., 2008); or reported a facilitation (Sakai et al., 2002). Furthermore, the causal role of the left IFG in the encoding of grammatical gender in neurologically normal observers has not been investigated. This was one objective of the present study. A second objective was to investigate whether distinct neuronal representations within the region respond preferentially to different classes of grammatical gender. If this is the case, one should be able to differentially modulate the encoding of masculine and feminine grammatical gender.

Here we used a verbal satiation paradigm to investigate whether subpopulations of neurons within the region respond preferentially to different classes of grammatical gender. Verbal satiation is a “higher-level” adaptation phenomenon in which spoken repetition of a category name leads to a reduced access to that category (e.g. Smith, 1984, Smith and Klein, 1990, Fillenbaum, 1964, Pilotti et al., 1997, Shimokido, 2003, Lindquist et al., 2006). In the present study we used a verbal satiation paradigm to suppress the representations of either masculine or feminine word genders by having subjects read aloud the Italian word “masculine” or “feminine” for 45 s. They were then asked to classify Italian target nouns into living and nonliving words. If distinct gender-specific neural representations exist, satiation to a particular grammatical gender should induce an impaired detection of words belonging to the satiated gender relative to words of the nonsatiated gender. In contrast, there would be no gender-specific behavioral cost associated with satiation to a specific grammatical gender if such distinct representations do not exist. During this semantic task, TMS was applied over either the left IFG (i.e. Broca's area) or over its right hemisphere homologue (or not applied) to investigate whether the left IFG is the neural substrate of any behavioral satiation effect and thus establishing a causal link between grammatical gender and the left IFG activity.

Section snippets

Subjects

9 subjects (3 males and 6 females, mean age 24 years) with normal or corrected-to-normal vision at the University of Pavia took part in the experiment. Informed consent was obtained from all subjects. The experiment was approved by the local ethical committee of the University of Pavia.

Verbal satiation

Verbal satiation is a phenomenon in which repeating the name of a category leads to a reduced access to that category (e.g. Smith, 1984, Smith and Klein, 1990). In a typical satiation paradigm a category name is

Results

Accuracy in the semantic decision task was very high and did not significantly differ across TMS conditions (No TMS: 97.8%, Left IFG: 97.1%, Right IFG: 96.3%; F(2) = 1.8, p = 0.19). Fig. 2A shows the mean reaction times as a function of congruency to the satiated grammatical gender. There were no significant main effect of either TMS site (F(2,16) = 0.44; p = 0.653) or Congruency to the satiated gender (F(1,8) = 1.22; p = 0.3) but there was a significant interaction (F(2, 16) = 3.77; p = 0.046). Pair-wise

Discussion

Our objective was to investigate whether distinct neural representations exist within Broca's area for different classes of grammatical gender and our results support this view. Repeatedly exposing participants to the word “masculine” (or “feminine”) selectively increased reactions to masculine (or feminine) words in the semantic decision task even though the gender of the word was incidental to performing the task. The presence of this satiation indicates that the neural representations of

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