In the current study, we investigated whether intraindividual 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 condition and group with respect to 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. Further, the words they generated were rated as less associated with meanings implying own-body movement, whereas this was not true of other movement aspects. This appeared to be a mixed effect from the reduction of verbs, generally entailing high movement-relatedness, and less own-body movement relatedness of nouns. The group differences were no longer significant, when persons with PD were on DBS. 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 on-DBS state were in between those measured in the 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 groups [44]. In PD, growing hypokinesia changes existential circumstances, mostly 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 expectations [45–56]. 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 alone does not comprehensively explain the obtained result pattern.
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, imply high suppression demands for holding back all lexical candidates apart from the best-suited option. As this selection process was presumed to be a frontostriatal function, its impairment could underlie verb production problems in persons with PD [27, 29–31]. This would tie in with the finding that lowered verb use in persons with PD off-DBS was no longer significantly different from normal levels in the on-DBS condition, i.e., after partial normalization of striatal function. It further appears to tie in 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 production [57–59]. However, this concept does not explain the overall semantic result pattern.
In this regard, a second view deserves a mention. Word class and content-related findings could be considered as coherent consequences of a DBS-induced gain of mental concepts related to own-body movement, promoting an increase of verb use (i.e., of the use of words with high motor relatedness) along with a congruent semantic shift in nouns [18, 23–26]. Such a direct impact of motor system states on lexical operations is reminiscent of typical MC claims [2, 11, 13, 14]. Data potentially supporting such positions are controversially discussed, for example, the activation of motor cortical areas during action word processing in functional imaging [8, 60], possibly indicating ‘modal’ cognitive processing or, alternatively, a post-lexical phenomenon without functional relevance, as well as behavioral observations, such as the Action Sentence Compatibility Effect (ACE) [2, 10], highly cited and, at the same time, put into question for a lack of reproducibility (Papesh, 2015). 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-physiological state, observable as a rapidly evolving relief of clinical symptoms [61–64]. 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 on-DBS was quite in the middle between the off-DBS 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 on-DBS and persons without PD as well as within persons with PD on versus off DBS. Thus, whereas motor states may acutely impact on the processing of words, this effect seems altogether relatively subtle.
In sum, the results (abnormally low verb production together with decreased own-body movement-relatedness of nouns in PD off-DBS; normalization of these abnormalities in the on-DBS condition) are compatible with the idea that momentary motor system states impact on the availability or prevalence of corresponding mental concepts, traceable on the level of word output. This pattern, suggesting a relatively direct link between motor and lexical processing, ties in with basic MC positions. It further provides a framework of low verb generation in PD, in addition and complementary to the proposal of a dysexecutive basis of this finding. These considerations are cautiously formulated for a number of reasons. Importantly, there is no data for the German word corpus on lexical movement-relatedness, so that the semantics in question were derived from the ratings of a group of native German speakers, who were unaware of the data origin and the study aim, as done in a previous study [34]. The scale used for this purpose ranged from 0 to 10 (minimum to maximum relatedness) and, although lexical own-body movement-relatedness was on average about twenty-five percent higher in persons without PD than in persons with PD in the DBS-off state, this difference was small in absolute numbers, since it referred to overall low ratings (around 2). In this regard, it is worthwhile to note that the current aim was to study potential indications of motor-to-lexical interactions, be they weak or strong, but not to quantify potential effects. The explorative tests targeted two main questions, firstly, whether previous reports on low verb use in the context of DBS-treated PD could be confirmed and, secondly, if verb reduction was accompanied by diminished motor semantics in non-verbs. Indeed, the results suggest that this combination was given, but future trials might confirm it in further cohorts.
Overall, the current data suggest that PD influences formal as well as content aspects of word generation, susceptible to DBS of the STN. This and the particular nature of the semantic shift in PD is compatible with the view that interactions between motor and cognitive functions have relatively direct neuronal underpinnings. From a theoretical perspective, this is of interest in the context of the debate about the existence and nature of MC; under clinical aspects, the results raise the question whether certain cognitive changes in PD might be less separable from motor dysfunction than commonly assumed.