Tracing embodied word production in persons with Parkinson’s disease in distinct motor conditions

In the current study, we investigated whether intra-individual motor system state changes influenced semantic and formal aspects of word generation. Therefore, persons with PD on as well as off DBS and healthy participants performed a phonemic VF task, so that lexical output could be analyzed per DBS condition and group with respect to different dimensions of movement-relatedness and word class properties.

In comparison to healthy participants, persons with PD in the DBS-off condition produced fewer words and, within this decreased lexical output, proportionally fewer verbs. Concerning this verb production difference, it should be noted, however, that it referred to very few words per participant, since the large majority of words produced were non-verbs in both groups and DBS conditions (see Table 3). Further, the words persons with PD generated in the DBS-off condition were rated as less associated with meanings implying own-body movement, whereas this was not true of other movement aspects. The group differences were no longer significant, when persons with PD were in the DBS-on condition. Between DBS conditions, no statistical distinction of VF-related performance was shown, while motor change, as assessed by the UPDRS, was significant. On average, values for own-body movement-relatedness and verb use in the DBS-on state were in between those measured in the DBS-off state in persons with PD and the corresponding values in healthy participants.

Principally, altered semantics and verb use could be conceived as a phenomenon without a specific relation to PD brain pathology, since everyday living conditions alone can frame lexical properties of persons or groups47. In PD, growing hypokinesia implies existential change related to agent-based motor behavior, and gradual alignment of mental concepts traceable on lexical levels could simply be a response to permanent mismatch between actual experience and unrealistic expectations48,49,50,51,52,53,54,55,56,57,58,59. However, if changed word use in persons with PD were only based on this, it should—as a slow, learning-based adaptation to enduring change—be inert to short-lived motor functional shifts by intermittent DBS in/activation. Yet, only in the DBS-off, but not in the DBS-on condition significant differences of lexical semantics and word class use were identified in comparison to persons without PD. Therefore, this framework does not comprehensively explain the obtained result pattern. Further, it is important to note that persons with PD experience the DBS-off condition as uncomfortable and, therefore, distress as a factor of the current results cannot be ruled out. However, this would probably have impaired VF task performance globally, i.e., as a reduction of word production without a relation to a specific semantic movement dimension or lexical class.

Concerning effects of acute motor change on lexical properties, two views deserve particular mention. Firstly, in the context of DBS modulation of word class use was conceptualized in a non-MC account, viewing low verb generation as a dysexecutive symptom in PD. Based on the assumption that striatal processing is crucial for inhibitory operations in motor as well as cognitive behaviors, PD was proposed to impair the release of words with numerous grammatical alternatives, as is the case in verbs. In this view, co-activation of their variable conjugational forms at the beginning of the lexemic retrieval process, demand the inhibition of all lexical candidates apart from the best-suited option. As this inhibitory selection process was presumed to be a frontostriatal function, its impairment could underlie verb production problems in persons with PD27,29,30,31. In this sense, the partial normalization of striatal function by DBS could have effectuated that the difference of verb production between controls and persons with PD in the DBS-off condition became insignificant under active DBS. This seems also compatible with previous findings, demonstrating that DBS of the STN not only acts on motor processing, but also supports impaired language-related executive operations, such as conceptual switching during word production60,61,62. However, this concept does not include the particular semantic result pattern.

In this regard, a second view deserves a mention, in which both altered verb-generation and content-related findings are the consequence of a DBS-induced shift of mental concepts related to the acute functional gain of the motor system and, thus, the capacity to move. Note that the specific production differences between persons with PD in the DBS-off condition referred formally to the lexical class of verbs and semantically to own-body movement-relatedness. The latter finding cannot be easily explained as the result of reduced production of verbs as a grammatical class18,23,24,25,26, because in this case equivalent effects on the other dimensions of movement-relatedness should have occurred. However, reminiscent of typical MC claims, the group difference of word ratings was only significant for the DBS-off condition and diminished in the DBS-on state, suggesting partial normalization of the underlying processes. Thus, it rather reflected the specific ‘semantic impact’ of the motor system state change, particularly related to the ability to move one’s own body. Further, it should also be pointed out that word production took place in a physically inactive state, that is, while seating on a chair, so that the described semantic effect was not dependent on a particular use of the motor system. This is compatible with the idea that the modulation of motor physiology in itself influences mental concepts associated with active movement2,11,13,14.

Data potentially supporting MC positions are controversially discussed. For example, the activation of motor cortical areas during action word processing in functional imaging8,63 may indicate ‘modal’ cognitive processing or, alternatively, a post-lexical phenomenon without functional relevance, the Action Sentence Compatibility Effect (ACE)2,10 is highly cited and, at the same time, principally put into question for a lack of reproducibility13 , and so forth. Against this background, the current data are of interest, because DBS of the STN brings the motor network of persons with PD in a closer-to-normal physiological state, observable as a rapidly evolving relief of clinical symptoms64,65,66,67. As known from many other investigations, it approximately halved the motor UPDRS in persons with PD, so that—according to this scale—the average movement function in the DBS-on condition was quite in the middle between the DBS-off state and the motor condition of persons without PD. Of note, lexical differences became only significant contrasting the UPDRS-defined motor conditions 40 points away from each other, but not at the also significant 20-point-distances, prevailing between persons with PD in the DBS-on state and persons without PD as well as within persons with PD on versus off DBS. Thus, whereas motor states may acutely affect the processing of words, this effect seems altogether relatively subtle.

Given the study limitations, these considerations are formulated with all the necessary caution. First of all, there is no German word corpus on lexical movement-relatedness, so that the semantics in question had to be derived from the ratings of a group of native German speakers, unaware of the data origin and the study aim34. On the used scale from 0 to 10 average ratings ranged around 2, and the observed group-difference of own-body movement-relatedness between persons with PD in the DBS-off state and controls was 0.5. Whether this small effect as well as the tiny differences in verb production has practically important implications remains unclear. In this regard, future studies using spontaneous speech samples could analyze potential effects of DBS on semantic levels of natural language. At this point, the current finding, raised in the artificial context of a VF task, may be considered as a signal of conceptual interest in the outlined theoretical context. Eventually, it should also be noted that, even in the logic of MC, it seems difficult to formulate an estimate of the degree of lexical-semantic change as a function of the severity of PD, in which motor system change is not absolute, but occurs gradually coming from a physiological basis of movement processing. Further, it needs to be mentioned that a very low inter-rater reliability was obtained, although the different dimensions of movement-relatedness and the used scale were extensively explained and corresponding examples were given. Principally, this could indicate that the rating task was difficult to accomplish or instructions were poorly understood. However, given the specific pattern of data material and ratings, we consider as likely that different persons naturally make quite divergent motor associations with words that were produced without any movement-related instruction and therefore convey rather low motor semantics. Accordingly, individual scores of motor-relatedness were mostly low, so that even minor differences of lexical conceptualization, e.g., due to inter-individually variable lexical use or experience associated with words, may have strongly decreased the agreement between the ratings. This thought is illustrated in Table 5, showing five words with the highest and lowest ratings of own-body movement relatedness each, as well as five words given the corresponding median rating value. The categorization of words with maximum and minimum values is easy to follow, just as the position of words with median ratings in between these extremes. However, the latter words (on the altogether low rating median) leave a wide interpretation space with respect to motor associations, probably implying factors such as personal habits, skills, attitudes, etc. In this regard, Fig. 2 shows the individual rating results for three example words, representative of the scoring pattern in case of high, medium, and low average scores for own-body movement-relatedness. With respect to the median score example (‘apron’), either half of the raters did or did not see movement-relatedness in any of the categories (an apron might move when one puts it on, but can be considered as immobile as well, and so on). This heterogeneity might reflect different associations the raters had with words, which do not primarily imply movement semantics, but which are interpretable in this regard, with average ratings of movement-relatedness between very high and low scores. The stronger homogeneity of ratings for words with maximum and minimum scores probably indicates less ambiguity with respect to the presence or absence of motor-related meanings. In so doing, the intra-rater reliability was moderate, indicating that, on an individual level, the evaluation pattern across the different dimensions of movement-relatedness varied between words to a certain degree, but not completely, i.e., the connection of one dimension of movement-relatedness to the other dimensions was not arbitrary per rater. Altogether, the raters judged words produced in the DBS-off state as less own-body movement-related than words produced by controls, but the evaluation of the movement-relatedness of each particular word strongly varied between them. To support the idea that this result pattern reflects a systematic embodiment effect, tasks used in future experiments should aim at higher inter-rater agreements, possibly directly demanding the production of movement-related words.

Table 5 Words with highest, median or lowest ratings.
Figure 2
figure 2

Individual ratings of the middle words from the lists (Table 5) for ‘highest’, ‘median’, and ‘lowest’ average ratings of own-body movement-relatedness. Cross signs indicate the per-rater scores.

In sum, the results (abnormally low verb production together with decreased own-body movement-relatedness in persons with PD in the DBS-off condition; reduction of these differences to controls in the DBS-on condition) are compatible with the view that momentary motor system states impact on the availability or prevalence of corresponding mental concepts, traceable on the level of word output. In this formulation, interactions between motor and lexical processing could further be understood as a factor of low verb generation in PD, in addition and complementary to proposed dysexecutive underpinnings. The findings may serve as food for thought in the debate about the existence and nature of MC, but, of course, should be verified in further trials. With respect to the particular case of PD, they inspire to give some thought about the question whether certain cognitive sequelae of the condition might be less separable from motor dysfunction than commonly assumed.

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