Activations of ''motor'' and other non-language ... - Semantic Scholar

Brain and Language 89 (2004) 290–299 www.elsevier.com/locate/b&l

Activations of ‘‘motor’’ and other non-language structures during sentence comprehension Laurie A. Stowe,a,* Anne M.J. Paans,b Albertus A. Wijers,c and Frans Zwartsd b

d

a Department of Linguistics, Graduate School of Behavioral and Cognitive Neurosciences, University of Groningen, Groningen, The Netherlands PET Center University Hospital, Graduate School of Behavioral and Cognitive Neurosciences, University of Groningen, Groningen, The Netherlands c Department of Experimental Psychology, Graduate School of Behavioral and Cognitive Neurosciences, University of Groningen, Groningen, The Netherlands Department of Dutch Linguistics, Graduate School of Behavioral and Cognitive Neurosciences, University of Groningen, Groningen, The Netherlands

Accepted 26 August 2003

Abstract In this paper we report the results of an experiment in which subjects read syntactically unambiguous and ambiguous sentences which were disambiguated after several words to the less likely possibility. Understanding such sentences involves building an initial structure, inhibiting the non-preferred structure, detecting that later input is incompatible with the initial structure, and reactivating the alternative structure. The ambiguous sentences activated four areas more than the unambiguous sentences. These areas are the left inferior frontal gyrus (IFG), the right basal ganglia (BG), the right posterior dorsal cerebellum (CB) and the left median superior frontal gyrus (SFG). The left IFG is normally activated when syntactic processing complexity is increased and probably supports that function in the current study as well. We discuss four hypotheses concerning how these areas may support comprehension of syntactically ambiguous sentences. (1) The left IFG, right CB and BG could support articulatory rehearsal used to support the processing of ambiguous sentences. This seems unlikely since the activation pattern associated with articulatory rehearsal in other studies is not similar to that seen here. (2) The CB acts as an error detector in motor processing. Error detection is important for recognizing that the wrong sentence structure has been chosen initially. (3) The BG acts to select and sequence movements in the motor domain and in cognitive domains may serve to inhibit competing and completed plans which is not unlike inhibiting the initially non-preferred structure or ‘‘unchoosing’’ the initial choice when incompatible syntactic input is received. (4) The left median SFG is relevant for the evaluation of plausibility. Evaluating the plausibility of the two possibilities provides an important basis for choosing between them. The notion of the use of domain general cognitive processes to support a linguistic process is in line with recent suggestions that the a given area may subserve a specific cognitive task because it carries out an appropriate sort of computation rather than because it supports a specific cognitive domain. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Ambiguity resolution; Sentence processing; Cerebellum; Basal ganglia; Superior frontal gyrus

1. Introduction Sentence comprehension is a very complex task, which can vary in its cognitive demands according to the nature of the sentences and contexts involved. It is traditional to see language processing as involving a specialized brain system, consisting of a relatively small assemblage of specialized processing modules handling

* Corresponding author. Fax: +31- 50-363-6855. E-mail address: [email protected] (L.A. Stowe).

0093-934X/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S0093-934X(03)00359-6

specific parts of the process. The involvement of anterior and posterior language areas has been confirmed by many neuroimaging studies (e.g., Caplan, Alpert, & Waters, 1998; Stowe et al., 1998). However other evidence from neuroimaging shows that language and other cognitive domains such as music perception and motor imagery (Binkofsky et al., 2000; Koelsch et al., 2002) activate common regions. This can be explained if tasks which share subcomponents (in this example, sequencing) are processed more according to the specific type of computation than to the cognitive nature of the task as a whole (Doya, 2000).

L.A. Stowe et al. / Brain and Language 89 (2004) 290–299

In this article we will discuss the results of an experiment investigating the processing of syntactically ambiguous sentences. Most neuroimaging studies of sentence processing have focused on violations or complexity; few studies of ambiguity resolution have been published (but see Cooke et al., 2001). We have good cognitive models of the processing of these sentences based on behavioral and event-related potential experiments, but relatively little understanding of those areas in the brain which support specific aspects of this process; the experiment was designed to provide an initial localization of those areas of the brain which are activated during ambiguity resolution. Under the classical model, it would be predicted that these activations would most likely be in language areas such as BrocaÕs and WernickeÕs areas; this is not the result which we found. The results of this study thus provide a good example of activations during language processing of areas whose involvement is better explained in terms of more general processes. First let us consider the cognitive operations which are involved in processing syntactically ambiguous sentences. In a sentence such as The red drops. . ., drops can be either a noun or a verb. If the sentence continues . . .fell onto the floor, then drops is a noun; if it continues . . .onto the floor, itÕs a verb. Syntactic disambiguation may not occur for several words. However, in many cases, one of the potential syntactic structures is simpler or more frequent than the other, allowing an immediate selection on the basis of structural preference (e.g., Frazier, 1978; Spivey & Tanenhaus, 1998). Semantic plausibility may also be sufficient for a choice between the structures (e.g., The wood drops. . .). Choice between the two structures on the basis of syntactic and semantic factors is thus one aspect of processing these sentences (Stowe, 1991; Tanenhaus, Spivey-Knowlton, & Hanna, 2000). Secondly, later context may make it clear that the initial choice was wrong. In The red drops from the dye bottle onto the floor, it turns out that drops must be a verb, even though on the basis of the frequency of red as an adjective, it may have initially appeared that drops was probably a noun. When an error of this type is detected, reanalysis must occur, involving reactivation or reconstruction of the alternative structure. The goal of the current study was to identify candidate areas which might be involved in these processes of choice, error detection and reanalysis. Subjects read syntactically ambiguous sentences and unambiguous controls. By disambiguating to the less preferred structure, we ensured that subjects would carry out all three processes. To determine which of these candidate area carries out which component, further experiments are necessary, but comparison with what is known about the functions of the activated areas allows us to formulate hypotheses about the contribution of each area.

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2. Study 2.1. Subjects 16 Dutch native speakers with no known neurological or perceptual deficits (aged 19–47; mean ¼ 23; 8F, 8M) volunteered for the study after giving informed consent under a procedure approved by the University Hospital Medical Ethics committee. 2.2. Materials Each subject read lists of sentences while four PET scans were made. Two lists consisted of eight ambiguous Dutch sentences followed by several unambiguous fillers. Early in the sentence a word occurred which was ambiguous with regard to syntactic category. The immediately following context was consistent with either possibility so that the ambiguity remained unresolved for at least four words (similar to The red drops from the dye bottle onto. . . : in which the ambiguity is maintained through the phrase in bold and only then resolves, to the less preferred reading). A single word late in the sentence could only form a grammatically correct sequence within the less preferred alternative, defined operationally as the structure which was less frequently used to complete the ambiguous context in a pretest (e.g., Complete: The red drops from the dye bottle _________). A variety of category ambiguities were employed. In two control lists, unambiguous sentences were presented. These lists were matched with the ambiguous sentences in pretest plausibility, and in word length and logarithmic word frequency. The syntactic structures of the unambiguous sentences were the same as those of the ambiguous sentences after ambiguity resolution (e.g., a sentence like The girl came from the upstairs flat to the party). 2.3. Procedure Subjects were placed in a Siemens CTI 951/31 positron emission tomograph camera. At the beginning of each scan, 1.86 GBq H15 2 O was injected as a bolus in saline via a cannula placed in the right brachial vein. Measurement began 23 s. after injection and continued for 60 s. Subjects read one of the four lists of sentences described above, presented word by word in the center of a computer screen. Subjects were instructed to ‘‘read the sentences attentively for comprehension’’; no further task was carried out. The order of presentation was varied so the four sentence lists occurred equally frequently as first, second, third or fourth scan. The two ambiguous lists never occurred consecutively. Sentences began seven seconds before measurements were started. Each word remained on the screen for 750 ms. and was immediately replaced by the following word; this speed

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voxel fairly dorsal (Fig. 1, above left), right hemisphere caudate nucleus (Fig. 1, above right), right hemisphere posterior dorsal cerebellum (CB) (Fig. 1, bottom left) and left hemisphere superior frontal gyrus (SFG)(Fig. 1, bottom right). No increases were found to be more activated during reading of unambiguous sentences relative to ambiguous sentences.

was found to ensure comprehension in a pretest. Between sentences an asterisk appeared in the center of the screen for 1800 ms. 2.4. Data analysis Regional cerebral blood flow was estimated for each voxel within the field of view of the camera and rescaled to voxel size 2.2 2.2 2.4 mm. Using the Statistical Parametric Mapping programs (Wellcome Institute for Neuroimaging), data were corrected for movement between scans and the data were normalized into the stereotactic coordinate system of Talairach and Tournoux (1988) in order to align across subjects (Friston et al., 1995a). Since this alignment is unlikely to be entirely successful, a Gaussian filter was also applied (20 mm in the x and y dimensions and 12 in the z dimension); in addition to reducing noise, this filter spreads the effects of an activation spatially so that nearly aligned activations are more likely to coincide across subjects. Regional cerebral blood flow was then compared across the two conditions. Since multiple voxel-by-voxel comparisons were made, a correction comparable to the Bonferroni correction was used (Friston et al., 1995b). Additionally, the number of contiguous activated voxels at the threshold Z > 3:0 was also calculated. Since it is not likely that a large cluster of voxels will be activated by chance, a calculation was also made of the significance level of the size of the activation (Friston, Worsley, Frackowiak, Mazziotta, & Evans, 1994). In this article, activations will only be regarded as significant if: (1) the maximal voxel within an activation is significant at a corrected P < :05 or (2) has a significant extent of activation at P < :05.

3. Discussion While processing syntactically ambiguous sentences, readers must evaluate which possibility is more likely and inhibit the less probable analysis; if incoming material is inconsistent with the initial choice, the error has to be recognized and the alternative analysis will have to be reactivated. In the current study, we have shown that four areas of the brain (the left IFG, the right caudate nucleus, the right CB and the left median SFG) are more activated when these processes must be carried out than when unambiguous sentences are read. Only the left IFG has been classically associated with language processing. This area has been shown to be activated in a number of studies in which the complexity of syntactic processing is manipulated (e.g., Caplan et al., 1998; Stowe et al., 1998); it seems likely that this area is involved in linguistic processing of the ambiguous structures, although the area activated in this study extends somewhat higher than the area usually activated by syntactic manipulations. The left IFG is also involved in motor planning and articulatory rehearsal, which we will return to below. The role of the other three regions is more problematic and we will concentrate on them in this discussion. In the following discussion, we will first briefly review evidence from lesion and patient studies that the CB and basal ganglia (BG) may play some role in sentence processing. Second, we will consider what is known of the functions of these latter three areas and what these functions might contribute to comprehension of syntactically ambiguous sentences.

2.5. Results The areas in Table 1 showed significant increased blood flow during processing of ambiguous sentences: left hemisphere inferior frontal gyrus (IFG), primarily BA 45 extending into BA 44 and 9, with the maximal

Table 1 Areas more activated during the reading of ambiguous sentences than of unambiguous sentences Area

L inferior frontal gyrus (BA 45) R caudate R posterior dorsal cerebellum L superior frontal (BA 8/9)

Max voxel x

y

z

)48 18 38 )14

20 6 )80 36

28 16 )24 44

Z

Corrected P

Extent (in voxels)

P extent

4.70 4.60 4.28 4.30

.005 .007 .026 .024

854 296 631 709

.059 .433 .128 .097

Location of the maximal voxel is given in Talairach and Tournoux coordinates, in which X ¼ left ())/right(+) of midline; Y ¼ anterior (+)/ posterior()) to the anterior commissure; Z ¼ dorsal(+)/ventral()) to the plane of the anterior and posterior commissure; statistics are reported for the maximal voxel (Z-value and P-value corrected for multiple comparisons and for the probability of a cluster of voxels of this extent reaching the threshold of Z ¼ 3:0).


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Fig. 1. Areas activated by syntactically ambiguous sentences Areas of activation (marked with an arrow) are shown projected onto an MRI template in radiological convention (left ¼ right): Upper left, left inferior frontal gyrus; upper right, right basal ganglia; lower left, right posterior dorsal cerebellum; and lower right, left superior frontal gyrus.

3.1. Evidence for a role for the cerebellum and basal ganglia in sentence processing: A review of the literature 3.1.1. Cerebellum There have been a number of reports of productive and receptive agrammatism following cerebellar damage (see Mari€en, Engelborghs, Fabbro, & De Deyn, 2001, for a review). Cases showing syntactic symptoms typically involve right cerebellar lesions (Riva & Giorgi, 2000; although see Fabro, Moretti, & Bava, 2000, for some exceptions) and frequently show relatively good recovery. Morphosyntactic production errors and decreased mean length of utterance characterize these

cases; comprehension also tends to fail on sentences which depend on syntactic structure. One common explanation for sentence level deficits associated with cerebellar lesions is that they affect left frontal lobe function via diaschisis (damage in one area leading to hypoactivity in connected areas). However, in at least one case, it was explicitly shown that linguistic deficits accompanying cerebellar dysfunction were not coupled with frontal hypoperfusion, ruling out diaschisis (Gasparini et al., 1999). The current results suggest that for during comprehension of some sorts of ambiguous sentences, the CB plays a relatively ‘‘active’’ role itself, which also argues against

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a classic diaschisis interpretation of sentence comprehension deficits. 3.1.2. Basal ganglia A number of cases of language deficits following lesions ‘‘more or less limited’’ to the BG have also been reported in the literature (see Nadeau & Crosson, 1997; , for review). A number of reports include difficulties with sentence production and comprehension (Alexander, Naeser, & Palumbo, 1987;Fabbro, Clarici, & Bava, 1996; Hochsteinbach, Spaendonck, van Cools, Horstinck, & Mulder, 1998; Pickett, Kuniholm, Protopapas, Friedman, & Lieberman, 1998). Additionally, a number of studies have shown that patients with ParkinsonÕs, degenerative disease primarily affecting the BG, have difficulties with syntactic structure (Grossman, 1999; Lieberman et al., 1992). Although most attention has been directed to left BG lesions, Hochstein et al. (1998) found that damage on either side was equally likely to cause deficits in sentence comprehension and verbal fluency. 3.1.3. Why are the basal ganglia and cerebellum not consistently associated with language dysfunction? It is clear that lesions of the BG and CB do not consistently have consequences for sentence processing, which suggests that possibly damage must occur to a particular area within either structure. The CB in humans is a large structure with massive interconnectivity with the cortex. It can be expected that different parts of the CB participate in different cortical functions due to the exact interconnectivity of the region involved; this is concistent the fact that by far the majority of the lesions associated with language production and comprehension problems are to the right cerebellar hemisphere, which is interconnected to the left cerebral hemisphere. The BG likewise receives input from—and sends output via the thalamus to—multiple areas of the cortex. Several attempts have been made to define the effects of damage to specific regions in and around the BG, cf Alexander et al. (1987). However, it should be noted that Nadeau and Crosson (1997), limiting their inquiries to cases of left striatocapsular infarction, found that only about half of their patients showed any linguistic disturbance and that the nature of the disturbance was extremely variable in those who did, which is not consistent with this view. 3.2. A motor pathway? On hearing that the IFG, the CB and the BG are activated together, the first idea which comes to most peopleÕs minds is that they form parts of a motor pathway and that their function is motor-related. If the function is not obviously motor in nature, as in this study, one option is that this motor pathway supports a

form of working memory which is necessary for the task. Articulatory rehearsal is the most likely on the assumption that this pathway primarily supports motor processing. It is known that articulatory rehearsal supports some aspects of sentence processing, since articulatory suppression interacts with propositional complexity and/or center-embedding (Caplan & Waters, 2000; Withaar, 2002). In the current task, with word by word presentation at a relatively slow rate, working memory demands are likely to be particularly high and retrieval of preceding words in some format is necessary for revision. If tasks which involve articulatory rehearsal activate the same areas which are activated in the current study, it would provide evidence that articulatory rehearsal is indeed involved in syntactic disambiguation, probably for use in reanalysis. There are, however, several problems with this account of both the experimental and the lesion data. First, the right BG is not expected to be involved in a circuit with either left frontal lobe or right CB.1 Second, as can be seen in Table 2, a selection of articulatory rehearsal tasks typically activate both frontal and cerebellar areas somewhat similar to those seen in the current study. However, they also activate premotor 6 bilaterally, do not activate the BG and the activation of the CB is bilateral rather than unilateral, so that the global pattern is quite different from that found in the current study. Third, it has also been demonstrated that short term memory deficits can be seen following right cerebellar lesions without any apparent agrammatism (Silveri, di Betta, Filippini, Leggio, & Molinari, 1998), while Riva and Giorgi (2000) report sentence level comprehension problems in patients who were able to repeat complex sentences verbatim, also suggesting a dissociation between articulatory rehearsal and sentence processing deficits in cerebellar lesions. Taken together these facts suggest first, that if a motor-like pathway supporting working memory is involved here, it unlikely to include the BG and second, that the representation which is involved is not articulatory, but some other higher-order cognitive form of representation. If this hypothesis is to be interesting and explanatory, it is necessary to determine what form of representation is relevant. As we noted earlier, both the CB and the BG exhibit massive interconnectivity with various areas of the cortex. Their interaction with these areas is probably not necessarily motor-based, but rather dependent on the nature of the process in each cortical area. The strategy of considering the kind of computations which are 1 This lack of connectivity between left frontal and right basal ganglia also argues against Ullman et al.Õs (1997) account of basal ganglia involvement in agrammatism as resulting from a frontostriatal network. For this reason we will not discuss this theory further here.


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Table 2 Overview of activations reported for articulatory rehearsal studies Study

Left X

Inferior frontal gyrus Paulesu, Frith, and Frackowiak (1993) Awh et al. Exp 1 (1996) Smith, Jonides, and Koeppe, Exp 1 (1996) Awh et al. Exp 1 (1996) Smith et al. Exp 1 (1996) Awh et al. Exp 2 (1996) Smith et al. Exp 3 (1996) Fiez, Raife, Balota, Schwarz, and Raichle, Exp 1 (1996) Smith et al. Exp 2 (1996) Celsis, Agniel, Demonet, and Marc-Vergnes (1991)

Y

Z

)46 )55 )55 )44 )44 )42 )42 )29

2 3 3 12 12 17 17 25

16 20 20 22 22 22 22 4

)37 n.a.

44

20

Mean

)44

15

19

Premotor 6 Awh et al. Exp 1 (1996) Fiez et al. Exp 1 (1996) Awh et al. Exp 2 (1996) Awh et al. Exp 2 (1996) Smith et al. Exp 3 (1996) Awh et al. Exp 2 (1996)

)48 )48 )28 )28 )28 )24

)6 )6 1 1 1 3

40 40 52 50 52 52

Mean

)33

0

)28 )26

)62 )67

Cerebellum Smith et al. Exp 3 (1996) Smith et al. Exp 3 (1996) Smith et al. Exp 1 (1996) Awh et al. Exp 1 (1996) Awh et al. Exp 2 (1996) Awh et al. Exp 2 (1996) Smith et al. Exp 3 (1996) Fiez et al. (1996) Fiez et al. (1996) Paulesu et al., 1993 Mean

Comparison

Right X 48

Y

Z 4

12

Maintain letter lists–visual recognition Letter recognition–match Letter memory–match Letter recognition–match Letter memory–match N-back–plain match Verbal 2-back–match Maintain word list– fix Verbal n-back–spatial List learning–listening

26 24

3 3

50 52

48

24

2

50

)52 )50

24

)62

)45

33 33 33 28

)60 )60 )60 )60

)25 )25 )25 )38

)26

)67

)50

)30 )17 )9 )18

)49 )77 )47 )54

)45 )24 )22 )16

27 14

)63 )60

)14 )16

)22

)60

)37

27

)61

)27

Letter recognition–match Word list maintain–fix N-back–plain match N-back–rehearsal Verbal 2-back–match N-back–plain match

Verbal maintenance–verbal control Verbal maintenance–verbal control Verbal–verbal control Letter recognition–match N-back–search N-back–rehearsal Verbal maintenance–verbal control Maintenance–fixation Maintenance–fixation Letter list–visual control

Locations are organized into left and right hemisphere activations of two areas within the frontal lobe and the cerebellum. The location of the maximal voxel is given in Talairach and Tournoux coordinates (cf. Table 1) and the nature of the comparison which elicited the activation is shown in the righthand column.

carried out by the CB and BG in motor processing may reveal the nature of their contribution to other cognitive functions. Recent evidence suggests that their contribution in these domains can be dissociated into error monitoring in the CB and sequential processing in the BG (Jueptner & Weiller, 1998). 3.3. Cerebellum as error detector In motor tasks, the CB uses perceptual information to monitor plans generated by the cortex for errors (Molinari, Filippini, & Leggio, 2002). This function underlies the role of the CB in motor learning (e.g., activation decreases as a motor task is learned, Friston, Frith, Passingham, Liddle, & Frackowiak, 1992). One

possibility is that the CB is an error detector with regard to many sorts of cortical processes, that is, that the CB is well-suited for this sort of computation (Doya, 2000). Recently evidence for this monitoring function has been extended to another verbal domain. Fiez, Petersen, Cheney, and Raichle (1992) suggested that the activation of the right lateral CB in word generation tasks (e.g., verbal fluency, verb generation, stem completion, translation, synonym generation) are all due to the need to detect outputs which do not fit the criteria. Fiez et al. (1992) showed that a right cerebellar patient showed many errors in word generation tasks with no learning or automatization of the task over time. Desmond, Gabrieli, and Glover (1998) showed that the CB is particularly activated during stem completion when

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there are few compatible completions, so that most options generated by the cortex will be errors. Crucially Fiez et al. (1992) assumes that there is an input to the CB from the cortex which can be compared to the output in order to detect errors. For the word generation tasks, the criteria is more abstract than a motor representation. An error detection mechanism is also necessary for various aspects of sentence processing. In production, failure of monitoring for errors according to a syntactic criterion would lead to morphosyntactic errors, which are frequently seen in agrammatic cerebellar patients. Failures in comprehension of ambiguous sentences may also occur if errors are not detected efficiently. There is little definite evidence for this possibility, but it makes some clear, testable predictions about when cerebellar activation similar to that found in the current study will occur. For example, the posterior dorsal CB should not be activated when there is no evidence against the initially preferred structure of a grammatically ambiguous sentence. Further, any sentence with a similar ungrammaticality would be expected to activate this area. A number of experiments have been carried out in which ungrammatical sentences were presented to subjects. The CB has not typically been activated in these studies; however, the CB has not typically been scanned in these studies either. (Moro et al., 2001) who scanned the whole brain, report a right lateralized cerebellar activation for detection of morphosyntactic errors. Both these predictions should be tested further in future research. 3.4. Basal ganglia as selection device In the motor domain, the BG appear to play an important role in action selection (Bergman et al., 1998). The final output of the striatum via the globus pallidus is tonically inhibitory, diminishing the likelihood of any action occurring; an action is chosen by ‘‘inhibiting inhibition.’’ In normal function, there seems to be a winner takes all result in this disinhibition, so that only one action takes place (Bergman et al., 1998). In motor sequence planning, it is proposed that this process focuses effort on the current action (‘‘choosing’’) and that loops within the BG are responsible for the smooth change to the following action involving an element of ‘‘unchoosing’’ or re-inhibiting the first movement (Onlo-or & Winstein, 2001). From this viewpoint it is not surprising that BG lesions and ParkinsonÕs disease frequently lead to speech production errors (Lieberman et al., 1992; Pickett et al., 1998). More broadly, this sort of procedure would allow the BG to adjudicate between competing actions which are planned in various cortical systems or between competing plans within the same domain. ‘‘Action’’ selection certainly applies in cognitive domains other than motor

output planning (Vakil, Kahan, Huberman, & Osimani, 2000). Godbout and Doyon (2000) demonstrated that patients have more problems with irrelevant intrusions when describing a familiar sequence of actions (e.g., getting up in the morning) than either normal controls or frontal patients. ‘‘Action’’ selection is not even limited to sequencing. Copeland, Chenery, and Murdoch (2001) reported that both ParkinsonÕs and BG lesion patients had problems in selecting an appropriate meaning for a semantically ambiguous word in sentence context (e.g., He dug with the spade), showing priming from the irrelevant meaning much later than normals. Moretti et al. (2001) noted that ParkinsonÕs patientsÕ verbal fluency errors are frequently irrelevant intrusions and that subthalamic nucleus stimulation, which improves motor symptoms, also leads to a decrease in intrusions. Syntactically ambiguous sentences are clearly a phenomenon in which a selection has to be made. First, a choice is made when the ambiguity is recognized and there is sufficient evidence to make a decision. Inhibiting the irrelevant possibility is important to prevent confusion. Secondly, when it turns out that there is an error, it is necessary to ‘‘unchoose’’ the initially selected structure. The activation in the current study is consistent with a role for the right BG in one or both of these procedures. Recently Frisch, Kotz, von Cramon, and Friederici (2003) have shown that left BG lesion patients show no P600 to ungrammaticalities. The P600 is an ERP response which is normally associated with recognizing an error and attempting to reanalyze the sentence to ‘‘fix’’ it. This suggests that the activation seen in the current study may reflect some aspect of the reanalysis procedure (see also evidence from Friederici, R€ uschemeyer, Hahne, & Fiebach, 2003 that the left BG is activated by ungrammatical sentences). The evidence that making an initial choice for semantically ambiguous words is also slowed in ParkinsonÕs patients and right BG lesion patients (Copeland et al., 2001) suggests that the initial choice may also be supported by this area. The degree to which there are lateralization of these processes in the BG is an interesting one for future research. 3.5. Left median frontal lobe and evaluation A large number of studies using language stimuli have shown activation in the left median frontal lobe. The tasks used were relatively diverse and the location quite variable, so that it is not clear whether the same function should be attributed to all of these activations, Nevertheless some clear generalizations can be made, Generally four sorts of language studies (see Table 3) have given rise to left median frontal activations: (1) those comparing probabilistic reasoning to deductive reasoning, (2) those comparing anomaly detection with another


297

Table 3 Sentence and text level studies reporting activation in the median frontal lobe Study

X

Y

Z

Comparison

Bottini et al. (1994) Broere et al. (1997) Caplan, Alpert, and Waters (1999) Ferstl and von Cramon (2001) Fletcher et al. (1995) Gallagher et al. (2000) Goel, Grafman, Sadato, and Hallett (1995) Goel et al. (1995) Goel, Gold, Kapur, and Houle (1997) Gusnard, Akbudak, Shulman, and Raichle (2001) Gusnard et al. (2001) Maguire, Frith, and Morrism (1999) Osherson et al. (1998) Osherson et al. (1998) Stromswold, Caplan, Alpert, and Rauch (1996)

)12 )6 )2 )4 )12 )8 )12 )4 )12 )9 )3 2 )12 )14 )2

54 44 18 58 36 50 38 52 54 39 23 42 24 46 30

20 28 48 13 36 10 32 24 24 42 54 )22 44 32 48

)6

55

13

Sentence–word list (Plausibility–lexical decision) Plausibility judgment–grammaticality judgment Auditory object clefts–subject clefts (anomaly detection) Coherent paragraphs–incoherent Theory of mind stories–physical stories Theory of mind story–non-theory of mind Theory of mind vs inference of own theory of mind–semantic retrieval Inductive–deductive Judgment emotion vs episodic content Judgment emotion vs episodic content Coherent story–incoherent story Probability reasoning–logic Anomaly detection–logic and probability judgments Center-embedded–pseudoword sentences (plausibility–lexical decision) Evaluative > episodic > rehearsal

Zysset, Huber, Ferstl, and von Cramon (2002)

Location of the maximal voxel for each activation is given for each study in Talairach and Tournoux coordinates (cf. Table 1) and the nature of the comparison which elicited the activation is shown in the right hand column.

task such as ungrammaticality detection or lexical decision, (3) theory of mind stories in which subjects need to infer motivations as well as understanding physical events, and (4) several studies requiring judgment of emotional response. The activated conditions all require either some evaluation of plausibility or use of probabilistic inferences where the judgment is not very clear (Ferstl & von Cramon, 2001). Gusnard et al. (2001) suggest that the function of this area is to support recruitment of personal experience. In any case, the function of this area seems to support higher-level semantic process involved in evaluation of plausibility, whether or not it carries out such processes itself. The current study does not involve any explicit component of semantic evaluation. However, covertly, it does require the evaluation of the relative plausibility of the two potential structures to choose between them. Given the clear evidence that this area supports evaluation, it seems likely that this is the contribution it makes in the current task. One issue is the extent to which the activations reported here are epiphenomena. This activation may reflect increased eye movement during more difficult processing conditions (Stromswold et al., 1996). Most of the activations reported here appear too anterior to involve median wall frontal eye fields (in a selection of studies involving eye movements similar to that reported for articulatory rehearsal studies, the center of supplementary motor activation due to eye movements ranged from )14 to +17 mm y and from +42 to +58 mm z). Additionally, eye movements would be expected to be bilateral, while most of these activations are left lateralized. Indeed, many of them do not show much if any extension to the right hemisphere (cf. the current study

as shown in Fig. 1). Lastly, in the current study and the other from our lab (Broere et al., 1997), sentences were presented one word at a time in the middle of the screen, which should eliminate rescanning in difficult sentences.

4. Conclusion We have considered several hypotheses about the involvement of areas that are not classically considered to be language areas in sentence comprehension. The current study confirmed that the BG and CB can be actively involved in sentence processing under some specific circumstances, as suggested by patient data. The cognitive operations which are necessary to understand syntactically ambiguous sentences (selection of a structure on the basis of semantic plausibility, detecting input which does not match this choice and reanalysis of the structure) are consistent with recent suggestions that the BG and CB are involved in action selection and error detection within cognitive processes as well as in motor processing and that the left median frontal lobe is supports evaluation. More globally, this conclusion is consistent with recent suggestions that the involvement of a specific area in a process depends more on the nature of the computation which must be carried out than on the specific cognitive domain of the process which must be carried out.

Acknowledgments This stiudy was supported by a CBR grant from the University of Groningen and the PIONIER project The Neurological Basis of Language, granted by the

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Netherlands Organization for Scientific Research (NWO) to the first author Thanks to Bauke de Jong, Evelyn Ferstl and two anonymous reviewers for careful comments on the manuscript. Thanks to Paulien Rijkhoek and Jonneke Brouw for help with materials and running subjects, to Remi Schmeits for scanning, and Antoon Willemsen for help with analysis, and the PET Center for technical support. References Alexander, M. P., Naeser, M. A., & Palumbo, C. L. (1987). Correlations of subcortical CT lesion sites and aphasia profiles. Brain, 110, 961–991. Awh, E., Jonides, J., Smith, E. E., Schumacher, E. H., Koeppe, R. A., & Katz, S. (1996). Dissociation of storage and rehearsal in verbal working memory: Evidence from positron emission tomography. Psychological Science, 7, 25–31. Bergman, H., Feingold, A., Nini, A., Raz, A., Slovin, H., Abeles, M., & Vaadia, E. (1998). Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends in Neuroscience, 21, 32–38. Binkofsky, F., Amunts, K., Stephan, K. M., Posse, S., Schormann, T., Freund, H.-J., Zilles, K., & Seitz, R. J. (2000). BrocaÕs region subserves imagery of motion: A combined cytoarchitectonic and fMRI study. Human Brain Mapping, 11, 273–285. Bottini, G., Corcoran, R., Sterzi, R., Paulesu, E., Schenone, P., Scarpa, P., Frackowiak, R. S. J., & Frith, C. D. (1994). The role of the right hemisphere in the interpretation of figurative aspects of language: A positron emission tomography activation study. Brain, 117, 1241–1253. Broere, C. A. J., Stowe, L. A., Wijers, A. A., Mulder, G., Koster, J., & Vaalburg, W. (1997). A complex syntax processing area in the temporal cortex. Journal of Cerebral Blood Flow and Metabolism, 17(Suppl. 1), S265. Caplan, D., Alpert, N., & Waters, G. (1998). Effects of syntactic structure and propositional number on patterns of regional cerebral blood flow. Journal of cognitive Neuroscience, 10, 541–552. Caplan, D., Alpert, N., & Waters, G. (1999). PET studies of syntactic processing with auditory sentence presentation. NeuroImage, 9, 343–351. Caplan, D., & Waters, G. (2000). Verbal working memory and sentence comprehension. Brain and Behavioral Science, 22, 77–126. Celsis, P., Agniel, A., Demonet, J.-F., & Marc-Vergnes, J. P. (1991). Cerebral blood flow correlates of word list learning. Journal of Neurolinguistics, 6, 253–272. Cooke, A., Zurif, E. B., De Vita, C., Alsop, D., Koenig, P., Detre, J., Gee, J., Pi~ nango, M. M., Balogh, J., & Grossman, M. (2001). Neural basis for sentence comprehension: Grammatical and shorterm-memory components. Human Brain Mapping, 15, 80–94. Copeland, D. A., Chenery, H. J., & Murdoch, B. E. (2001). Discourse priming of homophones in individuals with dominant nonthalamic subcortical lesions, cortical lesions and ParkinsonÕs disease. Journal of Clinical and Experimental Neuropsychology, 23, 538–556. Desmond, J. E., Gabrieli, J. D. E., & Glover, G. H. (1998). Dissociation of frontal and cerebellar activity in a cognitive task: Evidence for a distinction between selection and search. Neuroimage, 7, 368–376. Doya, K. (2000). Complementary roles of basal ganglia and cerebellum in learning and motor control. Current Opinion in Neurobiology, 10, 732–739. Fabbro, F., Clarici, A., & Bava, A. (1996). Effects of left basal ganglia lesions on language production. Perceptual and Motor Skills, 82, 1291–1298.

Fabro, F., Moretti, R., & Bava, A. (2000). Language impairment in patients with cerebellar lesions. Journal of Neurolinguistics, 13, 173–188. Ferstl, E. C., & von Cramon, D. Y. (2001). The role of coherence and cohesion in text comprehension: and event-related fMRI study. Cognitive Brain Research, 11, 325–340. Fiez, J. A., Petersen, S. E., Cheney, M. K., & Raichle, M. E. (1992). Impaired non-motor learning and error detection associated with cerevellar damage. Brain, 115, 155–178. Fiez, J. A., Raife, E. A., Balota, D. A., Schwarz, J. P., & Raichle, M. E. (1996). A positron emission tomography study of the short-term maintenance of verbal information. Journal of Neuroscience, 16, 808– 822. Fletcher, P. C., Happe, F., Frith, U., Baker, S. C., Dolan, R. J., Frackowiak, R. S. J., & Frith, C. D. (1995). Other minds in the brain: a functional imaging study of ‘‘theory of mind’’in story comprehension. Cognition, 57, 109–128. Frazier, L. (1978). On comprehending sentences: Syntactic parsing strategies. Bloomington, IN: Indiana University Linguistics Club. Friederici, A. D., R€ uschemeyer, S.-A., Hahne, A., & Fiebach, C. J. (2003). The role of left inferior frontal and superior temporal cortex in sentence comprehension: Localizing syntax and semantic processes. Cortex, 13, 170–177. Frisch, S., Kotz, S. A., von Cramon, D. Y., & Friederici, A. D. (2003). Why the P600 is not just a P300: The role of the basal ganglia. Clinical Neurophysiology, 114, 336–340. Friston, K. J., Worsley, K. J., Frackowiak, R. S. J., Mazziotta, J. C., & Evans, A. C. (1994). Assessing the significance of focal activations using their spatial extent. Human Brain Mapping, 1, 214–220. Friston, K. J., Ashburner, J., Frith, C. D., Poline, J. B., Heather, J. B., & Frackowiak, R. S. J. (1995a). Spatial registration and normalisation of images. Human Brain Mapping, 2, 165–189. Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. B., Frith, C. D., & Frackowiak, R. S. J. (1995b). Statistical parametric mapping and functional imaging: A general linear approach. Human Brain Mapping, 2, 189–210. Friston, K. J., Frith, C. D., Passingham, R. E., Liddle, P. F., & Frackowiak, R. S. (1992). Motor practice and neurophysiological adaptation in the cerebellum: A positron tomography study. Proceedings of the Royal Society of London—Series B: Biological Sciences, 48, 223–228. ^ F., Brunswick, N., Fletcher, P. C., Frith, Gallagher, H. L., HappeA, U., & Frith, C. D. (2000). Reading the mind in cartoons and stories: an fMRI study of Ôtheory of mindÕ in verbal and nonverbal tasks. Neuropsychologia, 38, 11–21. Gasparini, M., Di Piero, V., Ciccarelli, O., Cacioppo, M. M., Pantano, P., & Lenzi, L. (1999). Linguistic impairment after right-cerevellar stroke: A case report. European Journal of Neurology, 6, 353–356. Godbout, L., & Doyon, J. (2000). Defective representation of knowledge in ParkinsonÕs Disease: Evidence from a script-production task. Brain and Cognition, 44, 490–510. Goel, V., Gold, B., Kapur, S., & Houle, S. (1997). he seats of reason? An imaging study of deductive and inductive reasoning. NeuroReport, 8, 1305–1310. Goel, V., Grafman, J., Sadato, N., & Hallett, M. (1995). Modeling other minds. NeuroReport, 6, 1741–1746. Grossman, M. (1999). Sentence processing ParkinsonÕs disease. Brain and Cognition, 40, 387–413. Gusnard, D. A., Akbudak, E., Shulman, G. L., & Raichle, M. E. (2001). Median prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proceedings of the National Academy of Sciences (USA), 98, 4259– 4274. Hochsteinbach, J., Spaendonck, K. P. M., van Cools, A. R., Horstinck, M. W., & Mulder, T. (1998). Cognitive deficits

L.A. Stowe et al. / Brain and Language 89 (2004) 290–299 following stroke in the basal ganglia. Clinical Rehabilitation, 12, 514–520. Jueptner, M., & Weiller, C. (1998). A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain, 121, 1437–1449. Koelsch, S., Giunter, T. C., von Cramon, D. Y., Zysset, S., Lohmann, G., & Friederici, A. D. (2002). Bach speakes: A cortical ‘‘language-network’’serves the processing of music. Neuroimage, 17, 956–966. Lieberman, P., Kako, E., Friedman, J., Tajchman, G., Feldman, L. S., & Jiminez, E. B. (1992). Speech production, syntax comprehension, and cognitive deficits in ParkinsonÕs disease. Brain and Language, 43, 169–189. Maguire, E. A., Frith, C. D., & Morrism, R. G. M. (1999). The functional neuroanatomy of comprehension and memory: The importance of prior knowledge. Brain, 122, 1839–1850. Mari€en, P., Engelborghs, S., Fabbro, F., & De Deyn, P. P. (2001). The lateralized linguistic cerebellum: a review and a new hypothesis. Brain Language, 79, 580–600. Molinari, M., Filippini, V., & Leggio, M. G. (2002). Neuronal plasticity of interrelated cerebellar and cortical networks. Neuroscience, 111, 863–870. Moretti, R., Torre, P., Antonello, R. M., Capus, L., Gioulis, M., Marsala, S. Z., Cazzato, G., & Bava, A. (2001). Effects on cognitive abilities following subthalamic nucleus stimulation in ParkinsonÕs disease. European Journal of Neurology, 8, 726–727. Moro, A., Tettamanti, M., Perani, D., Donati, C., Cappa, S. F., & Fazio, F. (2001). Syntax and the brain: Disentangling grammar by selective anomalies. Neuroimage, 13, 110–118. Nadeau, S. E., & Crosson, B. (1997). Subcortical aphasia. Brain and Language, 58, 355–402. Onlo-or, S., & Winstein, C. J. (2001). Function of the ÔdirectÕ and ÔindirectÕ pathways of the basal ganglia loop: Evidence from reciprocal aiming movements in ParkinsonÕs disease. Cognitive Brain Research, 10, 329–332. Osherson, D., Perani, D., Cappa, S., Schnur, T., Grassi, F., & Fazio, F. (1998). Distinct brain loci in deductive versus probabilistic reasoning. Neuropsychologia, 36, 369–376. Paulesu, E., Frith, C. D., & Frackowiak, R. S. J. (1993). The neural components of the verbal component of working memory. Nature, 362, 342–344. Pickett, E. R., Kuniholm, E., Protopapas, A., Friedman, J., & Lieberman, P. (1998). Selective speech motor, syntax and cognitive deficits associated with bilateral damage to the putamen and the head of the caudate nucleus: A case study. Neuropsychologia, 36, 173–188.

299

Riva, D., & Giorgi, C. (2000). The cerebellum contributes to higher functions during development: Evidence from a series of children surgically treated for posterior fossa tumours. Brain, 123, 1051–1061. Silveri, M. C., di Betta, A. M., Filippini, V., Leggio, M. G., & Molinari, M. (1998). Verbal short-term store rehearsal system and the cerebellum. Brain, 112, 2174–2187. Smith, E. E., Jonides, J., & Koeppe, R. A. (1996). Dissociating verbal and spatial working memory using PET. Cerebral Cortex, 6, 11–20. Spivey, M. J., & Tanenhaus, M. K. (1998). Syntactic ambiguity resolution in discourse: Modeling the effects of referential context and lexical frequency. Journal of Experimental Psychology: Learning, Memory, Cognition, 24, 1521–1543. Stowe, L. A. (1991). Ambiguity resolution: Behavioral evidence for a delay. In Proceedings of the 13th annual meeting of the cognitive science association.. Stowe, L. A., Broere, C. A. J., Paans, A. M. J., Wijers, A. A., Mulder, G., Vaalburg, W., & Zwarts, F. (1998). Localizing cognitive components of a complex task: Sentence processing and working memory. NeuroReport, 9, 2995–2999. Stromswold, K., Caplan, D., Alpert, N., & Rauch, S. (1996). Localization of syntactic comprehension by positron emission tomography. Brain and Language, 52, 452–473. Talairach, J., & Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. Thieme Medical Publishers.. Tanenhaus, M. K., Spivey-Knowlton, M. J., & Hanna, J. E. (2000). Modeling thematic and discourse context effects with a multiple constraints approach: Implications for the architecture of the language comprehension system. In M. W. Crocker & M. Pickering (Eds.), Architectures and mechanisms for language processing (pp. 90–118). New York, NY, US: Cambridge University Press. Ullman, M. T., Corkin, S., Coppola, M., Hickok, G., Growden, J. H., Koroshetz, W. J., & Pinker, S. (1997). A neural dissociation within language: Evidence that the mental dictionary is part of declarative memory, and that grammatical rules are processed by the procedural system. Journal of Cognitive Neuroscience, 9, 266– 276. Vakil, E., Kahan, S., Huberman, M., & Osimani, A. (2000). Motor and non-motor sequence learning in patients with basal ganglia lesions: The case of serial reaction time (SRT). Neuropsychologia, 38, 1–20. Withaar, R. G. (2002). The role of the phonological loop in sentence comprehension. Groningen: GRODIL (Groningen Dissertations in Linguistics). Zysset, S., Huber, O., Ferstl, E., & von Cramon, D. Y. (2002). The anterior frontomedian cortex and evaluative judgment: An fMRI study. NeuroImage, 15, 983–991.