Thematic role assignment in the posterior parietal cortex: A TMS study

Thematic role assignment in the posterior parietal cortex: A TMS study

Author’s Accepted Manuscript Thematic role assignment in the posterior parietal cortex: A TMS study Chiara Finocchiaro, Rita Capasso, Luigi Cattaneo, ...

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Author’s Accepted Manuscript Thematic role assignment in the posterior parietal cortex: A TMS study Chiara Finocchiaro, Rita Capasso, Luigi Cattaneo, Arianna Zuanazzi, Gabriele Miceli www.elsevier.com/locate/neuropsychologia

PII: DOI: Reference:

S0028-3932(15)30141-X http://dx.doi.org/10.1016/j.neuropsychologia.2015.08.025 NSY5709

To appear in: Neuropsychologia Received date: 16 March 2015 Revised date: 4 August 2015 Accepted date: 24 August 2015 Cite this article as: Chiara Finocchiaro, Rita Capasso, Luigi Cattaneo, Arianna Zuanazzi and Gabriele Miceli, Thematic role assignment in the posterior parietal cortex: A TMS study, Neuropsychologia, http://dx.doi.org/10.1016/j.neuropsychologia.2015.08.025 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Title: Thematic role assignment in the posterior parietal cortex: A TMS study

Authors: Chiara Finocchiaro1, Rita Capasso3,4, Luigi Cattaneo2, Arianna Zuanazzi2, Gabriele Miceli1,2 1

Dipartimento di Psicologia e Scienze Cognitive, Università di Trento, Trento, Italy; 2Center for Mind/Brain Sciences (CIMeC), Trento, Italy; 3Fondazione Santa Lucia IRCCS, Roma, Italy; 4S.C.A. Associati, Roma, Italy

Affiliations institution(s) at which the work was performed: Università degli Studi di Trento Via Matteo del Ben 5/b, 38068 Rovereto (TN), Italy

Corresponding author: Chiara Finocchiaro Dipartimento di Psicologia e Scienze Cognitive Corso Bettini 31, 38068 Rovereto (TN), Italy e-mail: [email protected] Tel:++39 0464-808678; Fax:++39 0464-483554

Short title: Thematic roles in the parietal cortex

Key words: transcranial magnetic stimulation; brain mapping; natural language processing; posterior parietal lobe; thematic role assignment; reanalysis. Abstract: Verbs denote relations between entities acting a role in an event. Thematic roles are essential to the correct use of verbs and involve both semantic and syntactic aspects. 1

We used repetitive Transcranial Magnetic Stimulation (rTMS) to study the involvement of three different left parietal sites in the understanding of thematic roles. In a sentence-topicture matching task, twelve participants were asked to judge whether or not a given picture matched with a written sentence. Pictures represented simple reversible actions, and sentences were in the active or passive diathesis. Whereas both active and passive sentences require the correct encoding of thematic roles, passives also imply thematic reanalysis, as the canonical order of thematic roles is systematically reversed. The experiment was divided in three sessions. In each session a different parietal site (anterior, middle, posterior) was stimulated at 5 Hz in an event-related fashion, time-locked to the presentation of visual stimuli. Results showed increased accuracy for passive sentences following posterior parietal stimulation. The effect appeared to be (a) TMS-related, as no effect was observed in a control, no-TMS experiment with eighteen new participants; (b) independent from semantic processes involved in word-picture association, as no TMS-related effects were observed in a pictureword matching task. We interpret the results as showing that the posterior parietal site is specifically involved in the assignment of thematic roles, in particular when the correct interpretation of a sentence requires reanalysis of temporarily encoded thematic roles, as in passive reversible sentences.

1. Introduction For a long time, a sharp distinction has been drawn between anterior and posterior perisylvian areas as regards their role in sentence comprehension. Traditionally, anterior areas of the left hemisphere, and in particular Brodmann areas 44 and 45, referred to jointly as Broca’s area, have been considered to be responsible for –or at least involved in– virtually all syntactic operations related to verb and sentence processing (e.g., Rogalski et al., 2008; Carreiras et al., 2007; Hagoort, 2005; Friederici, 2002; Grodzinsky, 2000). By contrast, more posterior areas 2

including superior and middle temporal gyri and the inferior parietal lobule have been deemed critical for a vast range of computations that include storage and retrieval of semantic representations as well as verbal working memory processes (e.g., Fiebach et al., 2007; Jonides et al., 1998; Hart and Gordon, 1990; Warrington, 1975). In the past few years, this dichotomy has been questioned by a number of neuroimaging studies showing that parietotemporal regions are involved in the access to verb argument structure, and that activation in these regions varies as a function of argument structure complexity (Thompson et al., 2007; Palti et al., 2007; Shetreet et al., 2007; Bornkessel et al., 2005; Ben-Shachar et al., 2003). Computing argument structure is essential for the correct production and understanding of a verb, and involves both semantic and syntactic aspects. As a pretheoretical cover term and independently of idiosyncratic conceptions of specific orientations, “argument structure” captures the idea that verbs denote relations between entities, and that their role in the event is completely independent of the specific words used (Andrews, 1988; Comrie, 1993; Alsina, 2006). For instance, the verb valuate presupposes someone who does the action (the agent) and someone/something receiving that action (the patient or theme). Therefore, the frame of the verb valuate would be:

(1)

a. subcategorization: valuate V [NP]

b. argument structure: valuate

Thus, the correct comprehension of a verb argument structure entails the correct computation of the syntactic frame in which the verb may appear and the assignment of thematic roles to the participants that may be involved in the specified event (i.e., if they are agent, experiencer, theme, goal).

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A number of cues may help sentence comprehension and thus the correct processing of thematic roles, even when syntax is impaired. These cues may be semantic or probabilistic. Probabilistic cues mainly concern linear order. For instance, in English the agent often comes as the first element in a sentence. Consider as an example the sentence:

(2)

Linda eats the apple

In (2), even if the argument structure of the verb eat is not correctly retrieved, Linda can still be correctly identified as the agent, simply by appealing to a linear order cue (i.e., first element = agent). This strategy no longer works when the agent is in a different position. A typical case is that of passive sentences. The passive of (2) is:

(3)

The apple is eaten by Linda

The strategy first element = agent would lead to incorrectly interpreting the apple as the agent, which is clearly not the case. However, an interpretation along these lines is normally prevented by what is generally known about things in the world. That is, since we know that normally apples do not eat people, we end up with the correct interpretation of Linda as the agent of the action, even in the case of impaired syntax. Indeed, syntactic abilities are crucial for the identification of thematic roles when both probabilistic cues related to linear order and conceptual-semantic cues tied to encyclopedic knowledge cannot be used or when, if used, they would lead to misinterpreting the sentence. This condition is met by passive reversible sentences:

(4)

The girl is punched by the boy 4

Since in (4) both participants can in principle perform the punching action (this is the reason why sentences like (4) are called reversible), conceptual cues are unavailable. On the other hand, the linear order cue would lead to the wrong interpretation of the girl as the agent of punch. Note that the linear order cue could still work when reversible sentences are in the active diathesis. In:

(5)

The boy punches the girl

the boy is both the first element in the sentence and the agent of punch. In essence, if we were to represent sentence complexity on a scale, we would have:

(6)

Nonreversible Active > Reversible active > Nonreversible passive > Reversible

passive (Turner and Rommetveit, 1967)

There is clear evidence that subjects tend to interpret the first argument as the subject of the sentence and as the agent of the action denoted by the verb (Ferreira, 2003). Differently from active sentences, passive sentences systematically disconfirm the expectation set up by the order cue, thus forcing the listener to reanalyze temporarily encoded thematic roles. Since for reversible passives the reanalysis mechanism cannot be supported by semantic cues, the greater complexity of reversible passives accrues from the need to reanalyze thematic role assignment in the absence of either order or semantic cues. Linguistic theories vary with respect to the involvement of syntactic movement in passive sentences: Whereas movement-based accounts (e.g., Chomsky, 1981) state that identification of a passive structure requires the creation of a trace co-indexed with the grammatical subject, 5

lexical-thematic accounts (e.g., Pollard and Sag, 1994; Bresnan, 2000) do not. However, both accounts share the idea that noncanonical sentences like passive sentences trigger a process of thematic reanalysis, leading to a revision of an initial mapping of thematic roles. Reversible sentences, especially when the diathesis is passive, have been used to isolate the syntactic component in both neuropsychological and neuroimaging studies, in order to verify the functional organization and the neural correlates of the syntactic processes involved in sentence comprehension. A selective deficit in thematic role assignment was documented for the first time by Caramazza and Miceli (1991). Following vascular damage to the upper portion of the parietal lobe, patient EB showed a particularly pure dissociation between impairment of thematic role assignment and spared ability to process the morphological structure of sentences. In particular, both comprehension and production of semantically reversible sentences were impaired, significantly more for passive than active sentences. While Caramazza and Miceli (1991) focused on the contrast between the ability to assign thematic roles and to process morphosyntactic information in reversible sentences, other behavioral studies, involving brain-damaged or healthy participants, compared thematic role assignment accuracy by contrasting reversible sentences and other sentence types. Results showed that both aphasic and non-aphasic participants are slower and less accurate with passive than active reversible sentences in a sentence-picture matching task (Brookshire and Nicholas, 1980). More recently, Ferreira (2003) asked unimpaired participants to identify thematic roles in aurally presented sentences (e.g., Who was the doer?). Participants took longer and were more prone to misinterpret semantically reversible sentences, especially when grammatical structure deviated from the canonical subject-verb-object order (as is the case in reversible passives). Meyer et al. (2012), using the eye tracking-while-listening paradigm, asked aphasic and control participants to perform a sentence-picture matching task. 6

Participants listened to active and passive sentences and were presented with two pictures, the correct target and an alternative in which thematic roles were reversed. While participants selected the picture, their eye movements were monitored. The authors found that control participants showed an initial agent-first processing bias, followed by fixation on the correct picture in the vicinity of the verb in both active and passive sentences. Stated differently, in passive sentences, upon hearing N1 participants immediately looked at the picture in which N1 was the agent. A growing number of neuroimaging studies sheds light on the neurofunctional correlates of thematic role assignment. Some investigations found increased activations to verbs characterized by a more complex thematic structure or associated to more than one thematic grid. For example, Thompson et al. (2010), using a lexical decision task that included oneargument, two-argument, and three-argument verbs, found that a posterior perisylvian network is crucially engaged in processing information related to verb argument structure. Similar results were obtained by den Ouden et al. (2009), who found increased activity in posterior regions for naming transitive vs. intransitive verbs. In a lexical decision task, Meltzer-Asscher et al. (2013) compared simple verbs associated to one thematic grid, to verbs with alternating transitivity, which may be used transitively (with two thematic roles) or intransitively (with one thematic role), showing that alternating transitivity verbs yield significantly greater bilateral activation in the angular and supramarginal gyri, extending to the posterior superior temporal gyri. Other neuroimaging studies investigated thematic role assignment using sentences rather than single words. For instance, Richardson et al. (2010) found greater activation for reversible sentences in the left temporo-parietal boundary when participants silently listened to or read reversible and non-reversible sentences. In a sentencepicture matching task, Mack et al. (2013) found significantly greater activation for passive relative to active sentences in the inferior frontal gyrus bilaterally as well as in left temporo7

occipital regions. In a study of voxel-based lesion-symptom mapping in aphasia, Thothathiri et al. (2012) found a significant association between damage to temporo-parietal cortex and impaired sentence comprehension, even when controlling for phonological working memory. Thompson et al. (2013) used both verb naming and sentence generation tasks to train agrammatic patients in exploiting the argumental properties of verbs. They observed an improvement of verb production, that generalized to untrained verbs and recruited the same regions (posterior perisylvian, parietal and sensory-motor cortices bilaterally) as those associated with complex argument structure in healthy controls. Overall, despite different methods and results, available fMRI data converge with the neuropsychological literature in showing the involvement of left temporo-parietal regions in the assignment of thematic roles in reversible and passive sentences. However, even though fMRI provides neuroanatomical evidence with optimal spatial resolution, it only represents an indirect measure of brain activity. For this reason, in the present study we used Transcranial Magnetic Stimulation (TMS). This technique has an immediate effect on the activity of underlying cortical structures. Therefore, any behavioral modification that follows TMS is likely to be causally linked to changes in the activity of the stimulated brain structures. In a sentence-to-picture matching task, participants were asked to judge whether or not a picture matched with a sentence written below it. Pictures represented simple reversible actions involving humans or animals. In order to avoid the strategy first noun = subject, and force participants to analyze the verb before responding, sentences were presented without the first argument (e.g., baciano le figlie “[they] kiss the daughters”). This was possible because Italian, differently from English, is a pro-drop language (i.e., the subject may be omitted). The two roles in each sentence shared morphosyntactic features such as gender and number. In other words, even if the verb was the first element, its morphological marking may in principle apply to both participants. Mismatching sentences always used the same words as 8

the matching sentences, but the verb did not agree with the subject of the scene as represented in the picture (e.g., bacia “kisses” instead of baciano “[they] kiss”), or the thematic roles of agent and theme were reversed (e.g., baciano le mamme “[they] kiss the mothers” paired to a picture in which the mothers perform the kissing action on the daughters). Both matching and mismatching sentences could be in the active or in the passive diathesis. Thus, in order to perform the task correctly, participants had to identify the entities involved in the represented action and assign their thematic roles. Based on lesion data and on neuroimaging studies on healthy individuals, we predicted that TMS over parietal sites would affect performance in the experimental task. We had no specific expectations regarding which sites in the parietal lobe would yield an effect, because lesion data show the involvement of a large slab of parietal cortex, and neuroimaging studies do not provide univocal indications, especially because the specific issues addressed by each study and, consequently, methods and procedures show a large variability. Therefore, we decided to stimulate three sites along the intraparietal sulcus: If the parietal site stimulated in a given session is crucial for the task, performance after its stimulation should differ from that observed after stimulation of other parietal sites or during a control condition, in which (a different group of) participants performed the task with no TMS. A word-picture matching task was also administered. In this task, participants had to judge whether or not the picture of an object matched the noun written below it. Nouns could be correct or semantically related (e.g., APPLE- orange). This task was chosen because it requires lexical-semantic processes but not thematic role assignment. Performance accuracy in this task should not be affected by TMS, as available evidence from lesion and neuroimaging studies does not assign the parietal lobe a significant role in the lexical-semantic processes required by single-word comprehension.

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2. Methods 2.1. Participants A total of thirty right-handed (Oldfield, 1971) Italian native speakers took part in the study. Of these, twelve (7 male; mean age: 25.8; range: 19-37) were assigned to the TMS experiment, and eighteen (4 male; mean age: 22.2; age range: 19-36) to the no-TMS (control) experiment. All participants had normal hearing and normal or corrected-to-normal vision. They were not informed of the purpose of the study until the end of the experiment. None had a history of neurological or psychiatric disorders. Written consent was obtained from each participant. Participants in the TMS group were preliminarily screened for any relative or absolute contraindication to TMS. The study was approved by the local ethics committee.

2.2. Materials 2.2.1. Word-picture matching task A set of 40 pictures of objects was selected (Snodgrass and Vanderwart, 1980). Each picture was presented twice, once with its correct name (matching condition), once with a semantically-related noun (mismatching condition). Participants had to judge by pressing two different keys whether or not noun and picture matched. Four blocks were created in which each picture appeared only once and the same number of matching and mismatching trials was presented.

2.2.2. Sentence-picture matching task Thirty-two pictures representing a reversible action were selected (Miceli et al. 2006; Capasso and Miceli, 2001). For an example, see Fig. 1. The thirty-two verbs used in the sentences were all transitive obligatory 2-place verbs (e.g., baciare ‘to kiss’) with the exception of three 10

optional transitives (applaudire ‘to applaud’, fischiare ‘to whistle’, sognare ‘to dream’). As we used reversible sentences, virtually all verbs allow for a reciprocal use (e.g., baciarsi ‘to kiss reciprocally’) but only four verbs may be used as direct reflexives (uccidere/uccidersi ‘to kill/to commit suicide’, vestire/vestirsi ‘to dress/to get dressed’, bagnare/bagnarsi ‘to bathe’, asciugare/asciugarsi ‘to dry’). All the verbs used are listed in Appendix A.



Each picture was presented four times: twice with a matching sentence (one active, one passive), twice with a mismatching sentence (one active, one passive), yielding a total of 128 picture-sentence trials divided in four blocks. Each picture appeared only once per block, each time paired with a different sentence. In each block, there were an equal number of conditions. Mismatching trials could be in the active or in the passive diathesis and included two equally frequent types of mismatch: sentences with a morphological foil or sentences with a thematic foil. The trials associated to Figure 1 are listed as an example in Table 1.



Sentences were approximately of the same length. However, given that the same stimuli were presented in the active and in the passive diathesis, passive sentences were systematically two or three syllables longer than active sentences. Thus, longer RTs for passive sentences could be due to the intrinsic complexity of the passive voice or to length. Particular care was taken to avoid verbs denoting spatial relations (e.g., precede, follow), because the processing of spatial representations may involve parietal regions (Amorapanth et al. 2010; Baumann and 11

Mattingley, 2014). Ten additional stimuli were used as practice trials before the experiment proper began.

2.2.3 Sentence validation In order to establish whether subjects perceived differences between the picture-sentence trials in the active diathesis and in the passive diathesis, a preliminary acceptability judgment test was conducted. Thirty-four adult native Italian speakers took part in the acceptability judgment task (14 F; mean age: 24,4; range: 20-32), which was administered via an online survey. Stimuli consisted of the same 32 picture-sentence pairs used in the experiment. For every picture, three possible types of sentence were presented to each participant: active, passive and filler. Participants were asked to answer the question Would you use this sentence to describe this picture? Would you describe the action this way? by rating each picturesentence pair on a 7-point Likert Scale. Participants rated pairs with active sentences significantly higher than pairs with passive sentences (t(34) = 5.36, p <.000). This result shows that participants prefer the active diathesis over the passive diathesis to describe the pictures, and suggests that when the agent–verb–object order is modified (or rather, when agent and object are presented in the reverse order), the sentence becomes less preferred. This conclusion is in line with previous studies on thematic role assignment (Ferreira, 2003; Meyer et al. 2012).

2.3. Procedure 2.3.1 TMS experiment The study entailed three testing sessions that took place on three different days in three different weeks. Overall, the experiment took 4-5 hours per participant. During each session participants underwent TMS over one of the three possible stimulation sites. The sessions 12

consisted of a 2-min training part followed by a 40-min experimental part. In the training part, participants were trained with the same type of stimuli and tasks used in the experiment, in order to familiarize with the experimental set-up and tasks. Training was completed before the proper experiment (TMS and control groups) and repeated at the beginning of each session (TMS group only). Each experimental session included a word-picture matching and a sentence-picture matching task. During the experiment, participants were seated on a comfortable chair in front of a computer monitor. They were asked to perform the task by pressing one of two keyboard buttons with their left hand (2-alternative forced choice). In each experimental session, the word-picture task was presented before the sentence-picture task. Both tasks were presented using E-Prime, counterbalancing blocks across participants according to a Latin-square design. The same procedure was used for both tasks. Each trial started with a fixation cross for 500 ms, immediately replaced by the stimulus. Each stimulus consisted of a picture presented simultaneously to a sentence (sentence-picture task) or a word (word-picture task). The picture remained on-screen for a maximum of 3000 ms (2500 ms for the word-picture task) and disappeared after the participant responded. The SOA was kept constant across participants. Participants were asked to decide by keyboard press whether or not picture and sentence or picture and word matched (they had to press the yes button for the matching trials and the no button for the mismatching trials). They were explicitly told to respond as quickly and accurately as possible. The response could be provided at any moment during the trial. Reaction times and accuracy were measured relative to stimulus onset.

2.3.2 No-TMS (control) experiment The TMS experiment demonstrated a clear effect of TMS, limited to passive sentences (see Results section). We interpreted these data as the result of posterior TMS facilitating the processing of passive sentences. However, to strengthen our interpretation we needed to 13

establish how participants responded to the same set of stimuli in the absence of any stimulation. Therefore, we ran a control experiment without TMS. The no-TMS (control) experiment was carried out in a single session, identical to one of the sessions in the TMS experiment.

2.4. Magnetic stimulation 2.4.1. MRI acquisition and co-registration Prior to the experiment, a high-resolution T1-weighted magnetization-prepared rapid gradient echo sequence (176 axial slices, in-plane resolution 256 × 224, 1-mm isotropic voxels, generalized autocalibrating partially parallel acquisition with acceleration factor = 2, time repetition = 2700 ms, time echo = 4.180 ms, time to inversion = 1020 ms, flip angle = 7°) scan of the brain of each participant was obtained using a MedSpec 4-T head scanner (Bruker BioSpin, Ettlingen, Germany) with an 8-channel array head coil. Stimulation sites were identified on individual brain reconstructions on the basis of macroanatomical landmarks. In particular, the intraparietal sulcus was identified and divided in two halves of similar length (about 3 cm on the scalp for each half). Stimuli were applied to the anterior part of the IPS (hereafter named A), to the middle part (M) and to the posterior part (P). Fig. 2 shows the location of the three stimulation sites in a representative participant. The three points were individually targeted in single blocks, on three different days. The order of the three blocks (one for each of the stimulated points) was counterbalanced across participants. Before each TMS session, the participant’s head, the TMS coil and the 3D reconstruction of brain and scalp from individual MRI images were coregistered in space by means of the BrainVoyager (Brain Innovation BV, The Netherlands) neuronavigation system using the Zebris ultrasound tracker (Zebris, Medical GmbH, Germany). Coil position was monitored online with the

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BrainVoyager (Brain Innovation BV, The Netherlands) neuronavigation system and adjusted to the target location based on reconstructions of individual brain anatomies.



2.4.2. Stimulation parameters Biphasic TMS pulses were delivered via a figure-of-eight coil (diameter 70 mm) and a Magstim rapid stimulator (the Magstim Company - UK) in trains of three stimuli at 5 Hz. Before the experiment, the individual visible resting motor excitability threshold (RMT) of stimulation was established as the lowest stimulation intensity applied over the primary motor cortex capable of evoking a visible twitch of the right hand on at least five out of ten consecutive stimulations. The stimulation intensity used during the experiment was set at 90% of the individual threshold. The stimulation intensity used during the experiment was set at 90% of the individual threshold (mean = 54.3% SD = 8.6% of maximum stimulator output intensity). The coil was attached to a mechanical arm fixed to the chinrest and placed tangentially to the skull. The magnetic stimulator was triggered by the E-Prime software through the parallel port. TMS was delivered in an event-related fashion, time-locked to the presentation of visual stimuli. The first of the three rTMS pulses was delivered at the onset of the target picture. The last pulse therefore occurred at 400 ms from the picture onset.

2.5. Data analysis Responses exceeding 2500 ms (word-picture matching task) or 3000 ms (sentence-picture matching task) were excluded from the analyses of both RTs and Accuracy.

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Inaccurate responses and responses above or below two standard deviations of the participant’s mean were also removed from RTs analysis, but were included in the accuracy analysis.

2.5.1 TMS experiment For the TMS experiment, we considered as dependent variables the RTs and the Accuracy. The two tasks were analyzed separately. The data from the word-picture matching task were analyzed by means of a 2-way repeated measures ANOVA with the factors CORRESPONDENCE (2 levels: matching vs. mismatching) and TMS (3 levels: anterior, middle and posterior). The data from the sentence-picture task were analyzed by means of a 3-way ANOVA with the factors CORRESPONDENCE (2 levels: matching vs. mismatching) and DIATHESIS (2 levels: active vs. passive) and TMS (anterior, middle and posterior). The same analyses were performed separately on RTs and Accuracy as dependent measures.

2.5.2 No-TMS (control) experiment In the no-TMS groups analyses were carried out in a way similar to the TMS group. The word-picture matching task data were analyzed by means of a 1-way repeated measures ANOVA with the factor CORRESPONDENCE (2 levels: matching vs. mismatching). The data from the sentence-picture task were analyzed by means of a 2-way ANOVA with the factors CORRESPONDENCE (2 levels: matching vs. mismatching) and DIATHESIS (2 levels: active vs. passive). The same analyses were performed separately on RTs and Accuracy as dependent measures.

2.5.3 d-prime analysis in the sentence-picture tasks

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A d-prime analysis was carried out for the sentence-picture matching task of both the TMS and the no-TMS experiments. Specifically, d-prime was calculated as Z(hit rate) - Z(false alarm rate), where Z is the inverse of the cumulative Gaussian distribution. In particular, Hits were represented by ‘yes’ responses to matching trials and False Alarms were represented by ‘yes’ responses to mismatching trials. d-prime values were calculated for each experimental condition, i.e. active and passive in the control experiment and active and passive in each of the three stimulation sites (anterior, middle and posterior) in the TMS experiment. In the no-TMS experiment d-prime scores in the active and passive conditions were compared between matching and mismatching trials by means of a two-tailed, paired-sample t-test. In the TMS experiment the d-prime scores were analyzed by means of a 2-way repeatedmeasures ANOVA with the factors DIATHESIS (2 levels: active vs. passive) and TMS (anterior, middle and posterior)

3. Results 3.1 TMS experiment 3.1.1 Word-picture matching task No responses were excluded from the Accuracy analysis. As for RTs analysis, 3.4% of the responses to the matching condition and 4.1% of those to the mismatching condition were excluded. Overall Accuracy (mean for all participants in all sites of stimulation) was 96% (SD: 4.3) and 96.5% (SD: 4) for the matching and the mismatching condition respectively. No significant effects (main effects or interactions) emerged from the error analysis. Conversely, the analysis of RTs showed that matching stimuli were responded to significantly faster than mismatching stimuli(significant main effect of CORRESPONDENCE,F(1,11) = 22.72, p = 0.001, but no

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CORRESPONDENCE by TMS interaction, F(2,22) = 1.96, p = 0.163). RTs are listed in Table 2.



3.1.2 Sentence-picture matching task Approximately 1.1% of the responses to both active and passive sentences were excluded from the Accuracy analysis; 4.3% of the responses to active sentences and 5.3% of the responses to passive sentences were excluded from the analysis of RTs. The analysis of error rates showed a main effect of CORRESPONDENCE (F(1, 11) = 23.35, p = 0.0005), meaning that matching stimuli showed an overall higher Accuracy compared to mismatching stimuli, a significant DIATHESIS by CORRESPONDENCE interaction (F(1, 11) = 12.66, p = 0.004) and a significant DIATHESIS by TMS interaction (F(2, 22) = 15.87, p = 0.00005), all other effects and interactions fell short of significance (p>0.2). The main effect of CORRESPONDENCE and the CORRESPONDENCE by DIATHESIS interactions were not analyzed further because they did not include the TMS factor and therefore were not of interest for the current experimental hypothesis. The significant DIATHESIS by TMS interaction (illustrated in Fig. 3) was unpacked into two one-way ANOVAs, one for passive sentences and one for active sentences, with the single factor TMS (3 levels: anterior, middle and posterior sites). The ANOVA on active sentences showed no effect of TMS (F(2, 22) = 1.36, p = 0.27) as shown in the left panel of figure 3. The ANOVA on passive sentences showed a significant effect of TMS (F(2, 22) = 4.38, p = 0.024), illustrated in the right panel of figure 3. Post-hoc comparisons between the data from the 3 stimulation sites were carried out with pairwise t-tests, with a threshold of significance corrected for the 3 comparisons (p = 0.017). Results showed that posterior TMS was associated with a significantly higher 18

accuracy than anterior TMS (t(11) = 2.95, p = 0.013). A significant difference, which does not however survive the multiple comparison correction, between the posterior and the middle site was also found (t(11) = 2.26, p = 0.045) and no difference was found between the anterior and the middle sites (t(11) = 0.029, p = 0.77). Furthermore, to account for active-passive comparison, we unpacked the significant DIATHESIS by TMS interaction (illustrated in Fig. 3) into three two-tailed, paired-sample ttests, one for each stimulation site. The t-tests showed a significant difference between active and passive sentences in the anterior site (t(11) = 2.58, p = 0.025) and in the posterior site, but in the opposite direction (t(11) = -4.30, p = 0.001), meaning that, compared to active sentences, Accuracy for passive sentences is significantly lower in the anterior site and significantly higher in the posterior stimulation site. No significant difference was found in the middle stimulation site (t(11) = 1.06, p = 0.308). See Fig. 3 for results.



The analysis of RTs showed that stimuli with active sentences were responded to significantly faster than stimuli with passive sentences (significant main effect of DIATHESIS, F(1,11) = 30.25, p = 0.000) and that matching stimuli were responded to significantly faster than mismatching stimuli (significant main effect of CORRESPONDENCE, F(1,11) = 9.03, p = 0.012). Moreover, a significant DIATHESIS by CORRESPONDENCE interaction (F(1,11) = 22.52, p = 0.001), but no DIATHESIS by TMS or CORRESPONDENCE by TMS interaction was found. A two-tailed, paired-sample t-test showed a significant difference between active and passive sentences (t(11) = -14.50, p = 0.000) in the matching condition. RTs are listed in Table 3.

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3.1.3 d-prime results d-prime analysis showed a significant DIATHESIS by TMS interaction (F(2,22) = 12.25, p = 0.000). Two-tailed, paired-sample t-tests were performed also in this case. The d-prime score was significantly higher for active sentences than for passive sentences in the anterior site (t(11) = 3.20, p = 0.008), and significantly lower for actives than for passives in the posterior site (t(11) = -3.44, p = 0.005). Moreover, for passive sentences the d-prime score was significantly lower in the anterior than in the posterior site (t(11) = -2.59, p = 0.025). No significant differences were found between the anterior and the posterior stimulation sites with active sentences. Higher d-prime scores indicate more accurate discrimination between matching and mismatching trials. The significant difference in d-prime scores between active and passive sentences in the posterior site and between passive sentences in the anterior and posterior sites are not driven by a significant drop in False Alarms, but by an increase in Hits for passive sentences in the posterior site (t(11) = -2.31, p = 0.041 and t(11) = -3.41, p = 0.017, respectively). See Table 4 for results.



3.2 No-TMS (control) experiment 3.2.1 Word-picture matching task Following the criteria reported in 2.5, 0.2% of the responses to the matching condition and 0% of the responses to the mismatching condition were excluded from the Accuracy analysis.

20

Based on the same criteria, 8.5% of the responses to the matching condition and 7.8% of the responses to the mismatching condition were excluded from RTs analysis. Overall Accuracy (mean for all participants) was 95.9% (SD = 2.8) for the matching condition and 96.8% (SD = 5.8) for the mismatching condition. No significant difference emerged from the error analysis. Overall RTs (mean for all participants) was 489,18 ms (SD: 120,65) for the matching condition and 545,36 ms (SD: 123,45) for the mismatching condition. RTs analysis showed that matching sentences were responded to significantly faster than mismatching sentences (t(17) = -3.97, p = 0.001).

3.2.2 Sentence-picture matching task One percent of the responses to active sentences and 3.6% of those to passive sentences were excluded from the analysis of Accuracy; 13.3% of the responses to active sentences and 14.4% of those to passive sentences were excluded from RTs analyses. The analysis of error rates showed a main effect of CORRESPONDENCE (F(1,17) = 14.08, p = 0.002), meaning that matching stimuli showed an overall higher Accuracy compared to mismatching stimuli, and a significant DIATHESIS by CORRESPONDENCE interaction (F(1,17) = 4.79, p = 0.043). A two-tailed, paired-sample t-test showed a significantly higher Accuracy for active than passive sentences in the matching condition (t(17) = 2.22, p = 0.040). Overall Accuracy (mean for all participants) for the matching condition was 96.8% (SD: 2.2) for active sentences and 94.3% (SD: 4.8) for passive sentences. The analysis of RTs showed that stimuli with active sentences were responded to significantly faster than stimuli with passive sentences (significant main effect of DIATHESIS, F(1,17) = 72.22, p = 0.000) and a significant DIATHESIS by CORRESPONDENCE interaction (F(1,17) = 11.20, p = 0.000). A two-tailed, paired-sample t-test showed a significant difference 21

between active and passive sentences (t(17) = -11.13, p = 0.000) in the matching condition and in the mismatching condition (t(17) = -2.25, p = 0.038) (RT are listed in Table 3). Finally, d-prime analysis showed no significant difference between active and passive sentences (t(17) = 1.19, p = 0.247).

4. Discussion The main finding of the present experiment was the selective improvement of Accuracy for passive sentences following stimulation of the posterior parietal site. Post-hoc analyses show that Accuracy on reversible passives was significantly higher than Accuracy on reversible actives when stimulation was delivered to the posterior site, and significantly lower when the anterior or middle parietal sites were stimulated. No TMS-specific effects were disclosed by the analyses of response latencies. It is important to stress that the observed performance pattern is not the result of a speed-accuracy trade-off, as significantly improved Accuracy for passives following stimulation of the posterior site is not associated to increased RTs in the same condition. Moreover, d-prime analyses support the finding of a selective improvement for passives in the posterior site: Indeed, d-prime score was higher for passive sentences in the posterior site than for active sentences in the same site, and lower for passive sentences in the anterior site than for passive sentences in the posterior site. Our interpretation of the effects of TMS depends on the assumption that in baseline conditions passive sentences are processed less accurately than active ones. However, the validity of this assumption was to be demonstrated on the present set of stimuli, hence we performed the control, no-TMS experiment. It should be made clear that we cannot directly compare the control group data to the experimental group data statistically, which reduces the quantitative utility of the no-TMS group, however, qualitative comparison confirms our hypothesis. Results from the no-TMS group confirmed that in the absence of stimulation 22

participants’ responses to active sentences were both faster and more accurate than to passive sentences, and d-prime scores did not differ significantly between the two conditions. As to the word-picture matching task, no TMS-related effects were observed. Thus, the effect found in the posterior site cannot be reduced to an interaction with the lexical-semantic processes involved in associating words to pictures independent of a syntactic context. Other rTMS studies have provided evidence supporting the hypothesis that the posterior parietal site is important for the encoding of thematic roles as well as for working memory processes (Romero et al., 2006; Papagno et al., 2007; Romero Lauro et al., 2010). In particular, Romero Lauro et al (2010) found reduced accuracy after rTMS of the inferior parietal lobule (corresponding to BA 40) for sentences that were syntactically complex or that were long but syntactically simple and for sentences whose interpretation relied on word order. They argued that sentence comprehension is a function of the phonological loop, and that left BA 40, corresponding to the short-term store, is recruited for the comprehension of complex sentences and for that of long sentences, regardless of complexity. Indeed, both short-term memory and thematic encoding are involved in the sentence-picture matching task used in the present study. In order to correctly assign thematic roles, participants must keep auditory-verbal information active by relying on their phonological store (Baldo and Dronkers, 2006). Thus, our results may reflect the involvement of the posterior parietal site in the assignment of thematic roles, or in working memory processes. Even though we cannot definitely discriminate between the two hypotheses, we are inclined to prefer the thematic role hypothesis, as it provides a straightforward account of the different results for active and passive sentences. Indeed, some aspects of thematic role assignment are specific for passive reversible sentences. In passives, there is a systematic mismatch between thematic roles and syntactic functions, as the syntactic function of subject does not correspond to the thematic role of agent, but to the thematic role of theme (for the assignment of thematic 23

roles to null subject pronouns in Italian, see Rizzi, 1986). As a consequence, the temporary interpretation of the subject as agent has to be reanalyzed. By contrast, reanalysis is not required by active sentences, as in this case syntactic functions match the expected thematic roles, and the first interpretation of the subject as agent is correct. On the other hand, the working memory account would have predicted a similar pattern for actives across the three sites, with an improvement of performance on P3. This expectation also follows from the view that one of the computational principles of the working memory system underlying sentence processing requires fast content-addressed access to item information, but not to serial order information (Lewis et al. 2006). That is, starting from the reasonable assumption that working memory is more involved for passives, it should still be necessary for actives - albeit to a lesser extent, unless one would claim that the part of working memory that we see in our results is exactly that part that is necessary for people to reanalyze passive sentence (but in that case, the reanalysis and the working memory accounts would be virtually undistinguishable). Contrary to the expectation, no TMS-specific effect emerged for active sentences. It is also possible that our results on passives may hold true for other types of noncanonical sentences. However, other types of non-canonical sentences have been shown to involve different points than our P3 in the fMRI literature on the topic (Cooke et al., 2001; Bahlman et al., 2007; Kinno et al., 2008; Shetreet and Friedmann, in press). In particular, Kinno et al. (2008) studied, among other canonical and non-canonical sentence types, a non-canonical variant of the Japanese passive (the ni-passive), that according to the authors, requires thematic reanalysis. The authors do not distinguish between reversible and non-reversible passives, but, as revealed by the types of stimuli used (two very similar stick figures on each trial and one of the following verbs: pull, push, scold, kick,hit, and call, where call is transitive in Japanese), passive sentences were all reversible. Results showed that ni-passives 24

shared with non-canonical object-initial scrambled sentences the activation in the dorsal region of the left inferior frontal gyrus (that is, a non-parietal area). On the other hand, nipassives, but not scrambled sentences, activated an area very similar to our P3. More generally, as it appears from the studies quoted above, other types of non-canonical sentences do not seem to activate parietal areas. With the necessary caution in the interpretation of results obtained with different tasks and methodologies, we believe that a generalization of our results to non-canonical sentences in general is not fully justified on the basis of previous literature. Thus, we interpret our results as showing that the posterior parietal site is specifically involved in the assignment of thematic roles, in particular when the correct interpretation of a sentence requires reanalysis of temporarily encoded thematic roles. Another possibility is that the TMS effect on the posterior parietal site results from the spatial representation of the actors in the sentence rather than from thematic role encoding per se. To support this possibility, independent evidence shows that parietal regions are involved in encoding spatial relations (Amorapanth et al. 2010; Baumann and Mattingley, 2014). It is quite possible that non-linguistic spatial representations play a role in the understanding of thematic relations in language (Chatterjee et al. 1995; Coslett, 1999) and that the posterior parietal area that turned out to be crucial in our study is implicated in encoding those representations. However, the effect documented in the present study cannot be accounted for in this way, as we carefully avoided verbs denoting spatial relations (e.g., precede, follow), and selected verbs for which the need for spatial encoding of the actors is not obvious (e.g., kiss, dream, help, lick, caress). One aspect that deserves further comment concerns the polarity of the observed effect. We showed that 5-Hz stimulation of the posterior parietal site improves performance on passive sentences in a sentence-picture matching task. High frequency rTMS (i.e., ≥ 5-Hz), is conventionally thought to produce interference effects on behavior when applied online and 25

facilitatory, albeit short-lasting, after-effects when applied offline. (Di Lazzaro et al. 2002). In the present work we stimulated the target cortex in the first 400 ms from the onset of the visual stimulus, while response times exceeded 1000 ms. The most parsimonious account of the rTMS-induced performance gain observed in the present study relies on the hypothesis that the posterior intraparietal site processes the relevant information after the rTMS train is delivered, i.e. during the facilitatory aftereffects of rTMS. Similar facilitatory effects of rTMS delivered during the early phase of a reaction time have been described (see for example De Pisapia et al. 2012). A less likely hypothesis involves the phenomenon known in neuropsychology as paradoxical functional facilitation (Sandrini et al. 2011). On this account, under baseline conditions, the posterior intraparietal region would inhibit the processing of passive sentences. By blocking its function via rTMS, as in a canonical virtual lesion approach (Ziemann, 2010), comprehension of passive sentences would be facilitated. The idea that the posterior parietal site is specifically involved in the assignment of thematic roles is fully compatible with the fMRI literature showing the involvement of temporoparietal regions in the processing of thematic roles, especially in reversible and passive sentences (Thompson et al. 2010; Richardson et al. 2010; Meltzer-Asscher et al. 2013; Mack et al. 2013; Thompson et al. 2013). Results are also consistent with lesion data (Thothathiri et al., 2012) showing a significant association between damage to temporo-parietal cortex and impaired comprehension of reversible sentences, as revealed by voxel-based lesion-symptom mapping in a large aphasic sample. These latter authors claimed that the temporo-parietal cortex may be critical for a particular aspect of sentence comprehension, namely the assignment of thematic roles using sentence structure, at least when comprehension is statically investigated by correlating a given pattern of impaired performance with lesions to a given brain structure. Our results complement theirs in showing the critical involvement of

26

parietal areas also when sentence comprehension is dynamically investigated using a technique that allows a fine-grained temporal resolution. Comparisons between our study and the investigations considered above allow further considerations. The cortical region stimulated in our experiment corresponds to posterior BA40/anterior BA7. With the limitations inherent in the precise localization of cytoarchitectonic BA areas (Amunts et al., 1999; 2000), and in the comparisons across studies that use different localizing techniques, this region is extremely close to that activated in Meltzer-Asscher et al’s (2013) fMRI study of alternating transitivity verbs and in the study by Yokoyama and collaborators (2007), that contrasted activations to passive vs active reversible sentences in Japanese. However, it lies posteriorly to the areas activated in other fMRI investigations of thematic role assignment (Thompson et al, 2010; Richardson et al., 2010; Mack et al., 2013; Thompson et al., 2013), and to the area of greatest lesion overlap in the study by Thothathiri et al (2012), that converge around BA40. Since we did not stimulate BA40, we cannot explicitly correlate our results with those of the just-quoted studies. Be this as it may, we do not claim that the processing of thematic roles is limited to the posterior parietal site. Thus, our findings do not contrast with studies showing that other sites are involved in thematic role encoding. They suggest that the posterior parietal site stimulated in our study is involved in a process that is critical for the comprehension of reversible passives reanalysis. Additional observations support the view that a left-hemisphere region encompassing BA40 and BA7 may play a crucial role for thematic role assignment in sentences requring reanalysis. In a PET study of working memory via an n-back task (Smith, Jonides, Marshuetz & Koeppe, 1998), activity in a portion of BA7 posterior and superior to the area stimulated in our rTMS experiment was proportional to the distance between probe and target (i.e., to working memory task demands). If thematic role assignment in passive sentences requires 27

reanalysis of sentence structure, which in turn presupposes storage of information in working memory, the region encompassing BA40 and BA7 might play a complex role in sentence comprehension. Its anterior portion (BA40) might be involved in thematic role assignment, and its posterior/superior portion (BA7) in phonological storage in working memory. The intermediate region stimulated in our study might allow the two processes to interact. Interestingly, the Yokoyama et al fMRI study (2007) yielded significantly greater activation for reversible passives than for reversible actives in an area that essentially overlaps with our posterior parietal site.

5. Conclusions The present study investigated the neural correlates of thematic role assignment by using repetitive Transcranial Magnetic Stimulation (rTMS). This technique was selected because it induces short-lived, but circumscribed, immediate and measurable behavioral changes. Therefore, it can provide complementary information to that obtainable by other neuroimaging techniques (e.g., fMRI), whose time resolution is lower. To our knowledge, this is the first TMS study to address the neurofunctional correlates of thematic role assignment. We showed that a posterior left parietal site is selectively involved in encoding thematic relations in passive sentences, possibly at the stage where the canonical order of thematic roles is reanalyzed.

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Appendix A. List of the verbs used in the sentences of the sentence-picture matching task abbracciare ‘to hug’, accarezzare ‘to caress’, accogliere ‘to welcome’, aiutare ‘to help’, annusare ‘to smell’, applaudire ‘to applaud’, asciugare ’to dry’, aspettare ‘to wait’, assalire to attack’, baciare ‘to kiss’, bagnare ‘to bathe’, chiamare ‘to call’, colpire ‘to hit’, fischiare ‘to whistle’, fotografare ‘to photograph’, guardare ‘to look [at]’, indicare ‘to point [to]’, 34

leccare ‘to lick’, legare ‘to tie’, minacciare ‘to threaten’, mordere ‘to bite’, pettinare to comb’, pizzicare to pinch’, salutare ‘to greet’, soccorrere ‘to succour’, sognare ‘to dream’, solleticare ‘to tickle’, spaventare ‘to frighten’, spiare ‘to spy [(up)on]’, uccidere ‘to kill’, urtare ‘to bump [into]’, vestire ‘to dress’.

Figure captions

Figure 1. Example of an experimental picture Figure 2. Location of the three stimulation sites in a representative participant (A = anterior site, M = middle site, P = posterior site) Figure 3. Response accuracy to active and passive sentences following rTMS stimulation to the anterior, middle and posterior parietal site.

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36

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Table 1 Examples of trials for each sentence type Sentence type Active

Example (They) (Subject, Agent) ‘(They) kiss the daughters’

Passive (They) (Subject, Theme) ‘(They) are kissed by the mothers’ Thematic foil (Passive)

(They) (Subject, Theme) ‘(They) are kissed by the daughters’

Morphological foil (Active)

(She) (Subject, Agent) ‘(She) kisses the daughters’

Baciano kiss Verb

le figlie the daughters Object, Theme

Sono baciate are kissed Verb

dalle mamme by the mothers By-Phrase, Agent

Sono baciate are kissed Verb

dalle figlie by the daughters By-Phrase, Agent

Bacia kisses Verb

le figlie the daughters Object, Theme

Table 2 Mean and Standard Deviation of RT (ms) for the word-picture matching task in the TMS experiment

Site of stimulation Middle Posterior

Anterior

Mean

Matching

371,53 (126,41)

379,42 (157,20)

365,23 (115,49)

372,06 (133,03)

Mismatching

403,77 (141,82)

418,74 (169,53)

416,58 (130,97)

413,03 (147,44)

Correspondence

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Table 3 Mean and Standard Deviation of RT (ms) for the sentence-picture matching task in the TMS and NoTMS experiments TMS experiment

No-TMS experiment

Anterior

Middle

Posterior

Active

1023,71 (356,10)

1067,81 (288,48)

1037,73 (241,24)

1288,95 (265,64)

Passive

1163,16 (400,11)

1218,65 (325,47)

1183,81 (248,54)

1458,30 (245,53)

Active

1142,11 (381,26)

1138,45 (297,28)

1137,82 (207,60)

1367,28 (292,05)

Passive

1152,33 (362,61)

1179.63 (310.06)

1174,14 (270,32)

1410,55 (293,12)

Matching

Mismatching

Table 4 Mean and Standard Deviation of d-prime scores for the sentence-picture matching task

Anterior Sentence type (diathesis)

Site of stimulation Middle Posterior

Active

3.48 (0.53)

3.39 (0.51)

3.16 (0.53)

Passive

3.03 (0.50)

3.24 (0.78)

3.64 (0.57)

Highlights

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    

In passive sentences, comprehension of thematic roles involves thematic reanalysis. We applied 5Hz rTMS to three different parietal sites. We used a sentence-picture matching task with active or passive sentences. Accuracy increased for passives after stimulation of the posterior parietal site. The posterior parietal site is involved in the process of thematic reanalysis.

40