45.1 Introduction
Stuttering and Parkinson’s disease (PD) are complex neurological conditions characterized by disrupted motor control, which prominently manifests in speech and walking impairments. Within these disorders, an intriguing parallel emerges as both exhibit untimely initiation or termination of motor commands, leading to distinctive motor impairments. Stuttering, with its blockades, sound and syllable repetitions, and prolongations, significantly disrupts the smooth and rhythmic flow of speech (Bloodstein et al., Reference Bloodstein, Ratner and Brundage2021). In contrast, PD presents with dysfunctional gait and balance, along with freezing episodes, posing challenges to maintaining a regular rhythm while walking (Grabli et al., Reference Grabli, Karachi and Welter2012; Kalia and Lang, Reference Kalia and Lang2015). These rhythmic alterations not only affect the motor functions but also extend to rhythm perception. Remarkably, they transcend the boundaries of specific motor effectors and encompass broader rhythmic domains. Therefore, it becomes crucial to explore the underlying mechanisms that contribute to these rhythmic disturbances across diverse motor behaviors and perceptual processes. In this chapter we try to unravel the hypothesis that motor deficits in stuttering and PD partly originate from alterations within the timing system responsible for temporal prediction (e.g., Schwartze and Kotz, Reference Schwartze and Kotz2013). Investigating the interplay between motor control and temporal processing in the two classes of disorders will help to shed light on shared mechanisms. Particular attention will be paid to rhythm-based interventions building on these shared mechanisms and potentially leading to innovative treatment strategies. In doing so, we adopt a multidisciplinary approach, integrating neurology, speech pathology, motor control, and cognitive neuroscience.
45.2 The Role of Rhythm in Developmental Stuttering
Neurodevelopmental stuttering is a childhood-onset speech motor disorder that significantly disrupts the flow of speech (ICD-11, 2023). It is reported since antiquity across languages and regions around the globe. It is more prevalent in young children (around 5–10% of children aged two–three years) compared to adolescents or adults (~1%) (Yairi and Ambrose, Reference Yairi and Ambrose2013). In approximately 80% of affected children, symptoms naturally disappear within a few months to two years after stuttering onset, often before puberty (Yairi and Ambrose, Reference Yairi and Ambrose2004). However, some individuals continue to stutter into adulthood. Risk factors for persistent stuttering include co-occurring neurodevelopmental speech or language disorders (e.g., dyslexia, developmental language disorder), a family history of stuttering (with heredity estimates of 40–80%), late onset of stuttering (> four years), and being male (Frigerio-Domingues and Drayna, Reference Frigerio-Domingues and Drayna2017; Singer et al., Reference Singer, Hessling, Kelly, Singer and Jones2020).
Stuttering hinders the flow of speech with involuntary sound and syllable repetitions and silent pauses (Guitar, Reference Guitar2012). While typical speech dysfluencies include pauses and repetitions, such as searching for words or correcting mispronunciations (Lickley, Reference Lickley and Redford2015), stuttering stands out by disrupting the start or continuation of speech, leading to irregular breaks in speech flow (Guitar, Reference Guitar2012). Stuttering is often associated with physical symptoms such as muscle tension, facial grimacing, and involuntary movements (Bloodstein et al., Reference Bloodstein, Ratner and Brundage2021).
The arrhythmic character of stuttering is shaped by the randomness of symptoms. One individual’s frequency and severity of symptoms can randomly change from mild to severe stuttering from one day or situation to the other (Tichenor and Yaruss, Reference Tichenor and Yaruss2021). The temporal unpredictability of symptoms within a speech segment is probably one of the main reasons why stuttering is seen as a disorder disrupting the natural rhythm of speech. Stuttering’s unpredictable nature tends to disrupt conversation flow, prompting interlocutors unfamiliar with this disorder to use correction strategies such as completing sentences, interrupting, or prematurely taking turns (Guitar, Reference Guitar2012). Conversely, people who stutter might employ avoidance tactics in conversations, such as changing or skipping words and using fillers to conceal stuttering or avoid taking turns (Tichenor and Yaruss, Reference Tichenor and Yaruss2019). These attempts from both sides to restore a smoother flow of conversation or conceal the stuttering are ultimately ineffective. The continuous struggle with self-expression can cause frustration, leading to speech avoidance, together with feelings of guilt, shame, and fear, which significantly affect their psychosocial well-being, and may result in isolation or depression, underscoring stuttering’s classification as a communication disorder (Bloodstein et al., Reference Bloodstein, Ratner and Brundage2021; DSM-5, 2013).
At the core, stuttering is believed to stem from malfunctioning speech motor planning. Various hypotheses share the idea that the timely initiation and termination of speech movements might be compromised because of faulty integration of information from the auditory and motor systems (Alm, Reference Alm2004; Chang and Guenther, Reference Chang and Guenther2020; Civier et al., Reference Civier, Bullock, Max and Guenther2013; Harrington, Reference Harrington1988; Max et al., Reference Max, Guenther, Gracco, Ghosh and Wallace2004; Smith and Weber, Reference Smith and Weber2017). The motor system’s predicted output may temporally not align with the actual auditory feedback, resulting in temporal conflicts and, ultimately, stuttering symptoms (Max et al., Reference Max, Guenther, Gracco, Ghosh and Wallace2004). Consequently, the motor system struggles to provide accurate timing cues for fluent speech production (Alm, Reference Alm2004). At the neuronal level, altered connectivity and structural changes in the auditory, motor control, and timing circuits, including the basal-ganglia-thalamo-cortical circuits, have been observed in individuals who stutter (Chang et al., Reference Chang, Erickson, Ambrose, Hasegawa-Johnson and Ludlow2008, Reference Chang, Zhu, Choo and Angstadt2015; Connally et al., Reference Connally, Ward and Pliatsikas2018; Kronfeld-Duenias et al., Reference Kronfeld-Duenias, Amir, Ezrati-Vinacour, Civier and Ben-Shachar2016; Sommer et al., Reference Sommer, Koch, Paulus, Weiller and Büchel2002). These changes affect speech production, auditory–motor learning, and information flow between left-hemisphere areas and subcortical structures (Chang and Zhu, Reference Chang and Zhu2013; Giraud et al., Reference Giraud, Neumann and Bachoud-Levi2008; Kell et al., Reference Kell, Neumann, Behrens, von Gudenberg and Giraud2018; see also Chang and Guenther, Reference Chang and Guenther2020). Structural alterations have also been reported in key structures within the left-dominant part of the networks (e.g., supplementary motor area, inferior frontal gyrus and premotor cortex, putamen and nucleus caudate; e.g., Beal et al., Reference Beal, Gracco, Brettschneider, Kroll and De Nil2013, Reference Beal, Lerch and Cameron2015; Chang and Guenther, Reference Chang and Guenther2020; Neef et al., Reference Neef, Anwander and Friederici2015).
If the general timing network plays a role in stuttering, why would only speech be affected? Indeed, studies have shown that individuals who stutter exhibit distinct patterns in tasks involving metronome tapping, displaying less consistency and accuracy compared to their fluent peers, particularly those with moderate to high stuttering severity (Falk et al., Reference Falk, Müller and Dalla Bella2015; Sares et al., Reference Sares, Deroche, Shiller and Gracco2019). Children who stutter also demonstrated weaker discrimination of musical rhythmic sequences, suggesting difficulties in generating an internal beat in both music and speech, at least in an English-speaking population (Wieland et al., Reference Wieland, McAuley, Dilley and Chang2015). These findings, in conjunction with neural observations, point towards the involvement of the broader timing network in stuttering.
45.3 Rhythm Disorders in PD
After Alzheimer’s disease, characterized by the gradual loss of cognitive function, memory impairment, and changes in behavior and personality, PD is the second most common neurodegenerative disorder, and the most common serious movement disorder (Hirtz et al., Reference Hirtz, Thurman and Gwinn-Hardy2007). There are about four million patients worldwide suffering from PD (Andlin-Sobocki et al., Reference Andlin-Sobocki, Jönsson, Wittchen and Olesen2005). The disorder is caused by the progressive loss of neurons in the substantia nigra, which disrupts dopaminergic projections to the basal ganglia (specifically, the caudate nucleus and putamen) and leads to the deregulation of basal ganglia-thalamo-cortical circuitry.
Three cardinal symptoms characterize PD, namely resting tremor, limb rigidity (stiffness and resistance to movement in the muscles, causing a reduced range of motion), and general slowness of movement and difficulty initiating and executing voluntary actions (bradykinesia/akinesia) (Jankovic, Reference Jankovic2008; Kalia and Lang, Reference Kalia and Lang2015; Samii et al., Reference Samii, Nutt and Ransom2004).
In addition to these cardinal symptoms, PD also presents with significant motor signs related to gait and balance. As PD progresses, the severity of these symptoms tends to increase (Bloem, Reference Bloem1992; Grabli et al., Reference Grabli, Karachi and Welter2012; Koller and Montgomery, Reference Koller and Montgomery1997). During the early stages, gait dysfunctions can be observed when patients engage in dual-task conditions, such as walking while simultaneously performing another task (e.g., speaking). These dual-task situations place demands on limited attentional resources and executive functions (Al-Yahya et al., Reference Al-Yahya, Dawes and Smith2011; Kelly et al., Reference Kelly, Eusterbrock and Shumway-Cook2012). Gait alterations in PD include smaller and less regular steps due to shorter strides, compensatory adjustments in cadence (steps/min) to account for reduced stride length, reduced gait velocity, as well as festination and freezing (difficulty in initiating or stopping gait when turning or approaching an object) (Giladi, Reference Giladi2001; Grabli et al., Reference Grabli, Karachi and Welter2012; Morris et al., Reference Morris, Iansek, Matyas and Summers1994, Reference Morris, Huxham, McGinley, Dodd and Iansek2001). All these alterations of walking lead to dysfunctional gait rhythm in PD. These deficits are a major cause of disability, hindering patients’ mobility and independence, and a growing economic burden for the healthcare system (Grabli et al., Reference Grabli, Karachi and Welter2012).
Notably, rhythm disorders apparent in Parkinsonian gait extend across motor domains. Rhythm disorders in PD are also found in orofacial rhythmic coordination (e.g., in oral diadochokinesis tasks), where patients have difficulties in keeping a steady – isochronous – oral rhythm (Skodda et al., Reference Skodda, Flasskamp and Schlegel2010), and in tapping tasks when they have to tap their hand or finger at a regular rhythm or to an external rhythmic stimulus (Benoit et al., Reference Benoit, Dalla Bella and Farrugia2014; Bieńkiewicz and Craig, Reference Bieńkiewicz and Craig2015; Jones and Jahanshahi, Reference Jones and Jahanshahi2014). Rhythm disorders in PD manifest also in perceptual tasks, in the absence of motor output, such as extracting the beat from a musical sequence (Grahn and Brett, Reference Grahn and Brett2009; Tolleson et al., Reference Tolleson, Dobolyi and Roman2015). Only a few studies have investigated the relationship between rhythm variability across different motor domains in PD. Evidence suggests a correlation between rhythmic features of gait and speech in PD (Cantiniaux et al., Reference Cantiniaux, Vaugoyeau and Robert2010). Recent research from our laboratory demonstrates a tight relationship between the variability of motor actions across various effectors (e.g., finger tapping, gait, oromotor system) and impaired beat perception, suggesting that a central mechanism related to rhythm processing may contribute to rhythm motor disorders across domains (Dalla Bella, Reference Dalla Bella2022; Puyjarinet et al., Reference Puyjarinet, Bégel and Gény2019). Notably, these effects across motor domains, including speech production, are observed in spite of the variability of the rhythm class of language (French, English) (see also Chapters 11, 33, 30, 32, and 40); altogether these findings support the concept of a central disorder, referred to as “general dysrhythmia,” underlying rhythmic deficits in PD (Cantiniaux et al., Reference Cantiniaux, Vaugoyeau and Robert2010; Puyjarinet et al., Reference Puyjarinet, Bégel and Gény2019; Tolleson et al., Reference Tolleson, Dobolyi and Roman2015).
This parsimonious explanation of general rhythm disorders in PD is in keeping with the neuronal basis of the disease, involving basal ganglia-cortical circuitries (Factor and Weiner, Reference Factor and Weiner2008), which play a role in rhythm processing and temporal prediction (Grahn and Brett, Reference Grahn and Brett2007, Reference Grahn and Brett2009; Schwartze and Kotz, Reference Schwartze and Kotz2013). Indeed, the core neural circuitry impacted by PD, which includes the basal ganglia, premotor cortex, and pre-supplementary motor area, is also involved in rhythm perception and production (Chen et al., Reference Chen, Penhune and Zatorre2008; Coull et al., Reference Coull, Cheng and Meck2011; Dalla Bella et al., Reference Dalla Bella, Benoit and Farrugia2017; Grahn and Brett, Reference Grahn and Brett2007; Grahn and Rowe, Reference Grahn and Rowe2009; Repp, Reference Repp2005; Repp and Su, Reference Repp and Su2013).
45.4 Overlaps between Developmental Stuttering and PD
Despite significant clinical and age-related distinctions between stuttering and PD, both disorders share a dysfunction in the basal ganglia-cortical network, a critical component involved in rhythm processing and temporal prediction (see Table 45.1). This suggests that overlaps should be observed across the two classes of disorders. This section explores shared phenomena and mechanisms between PD and stuttering and highlights that both conditions can be considered as rhythmic-motor disorders, emphasizing their rhythmic aspects in addition to motor dysfunction.
| Stuttering | PD | |
|---|---|---|
| Disorder type | Neurodevelopmental | Neurodegenerative |
| Primary affected motor rhythm | Speech (syllabic rhythm, initiation, execution) | Gait (initiation and maintenance) |
| Other affected motor rhythms | Tapping (paced/unpaced) | Tapping (paced/unpaced) Oromotor coordination (diadocokinesis) Speech (dysarthria, stuttering) |
| Rhythmic perception affected? | Maybe (one study) | Yes |
| Similarities between stuttering and PD | ||
| Neural bases | Alterations in the basal ganglia-thalamo-cortical network | |
| Main underlying mechanisms | Impaired temporal predictions and less automatized/de-automatized motor patterns | |
| Benefits from | Enhancing temporal cues, auditory pacing, training of auditory–motor patterns | |
45.4.1 Stuttering in PD
Although dysarthria is the most prominent speech motor disorder in relation with PD (e.g., Duffy, Reference Duffy2019), stuttered dysfluencies are also found, in particular in more severe and longer-term cases of PD (Benke et al., Reference Benke, Hohenstein, Poewe and Butterworth2000; Gooch et al., Reference Gooch, Horne and Melzer2023). In the few studies available (see Gooch et al, Reference Gooch, Horne and Melzer2023, for a summary), estimates of new-onset stuttering in PD patients range between 4 and 53%. Individuals who had once remitted from childhood stuttering were also found to present stuttering again at the onset of PD (Shahed and Jankovic, Reference Shahed and Jankovic2001).
45.4.2 “Freezing of Gait” versus “Gluency” in Speech
Alm (Reference Alm2021) recently discussed similarities between gait freezing in PD and stuttering in the “inability to move forward in a movement sequence,” whether gait or speech. Freezing of gait implies a blockade appearing as a failure in gait initiation, or occurring abruptly while patients are walking; in the latter case, a sudden decrease of step length and increase of step frequency and step-to-step variability is observed prior to a complete blockade, which may lead to falling (e.g., Grabli et al., Reference Grabli, Karachi and Welter2012). For stuttering, the term “gluency” has been coined for the subjective experience of being stuck and unable to control the articulators as wished (Van Riper, Reference Van Riper1992).
45.4.3 Effects of Auditory Pacing
In developmental stuttering, we find “fluency-enhancing conditions” that can significantly reduce stuttering, sometimes to no stuttering symptoms at all. There are different forms of these conditions. Some of them temporarily change the way auditory feedback of speech is delivered (e.g., whispering, delaying auditory feedback, auditory masking with noise or music). Others provide auditory rhythmic cues or rhythmic enhancement (i.e., speaking with a metronome, singing, choral speech; Andrews et al., Reference Andrews, Howie, Dozsa and Guitar1982; Ingham et al., Reference Ingham, Bothe and Jang2009). However, the beneficial effect of fluency-inducing conditions wanes after stopping the cue or altered feedback. Interestingly, stuttering in PD has a long tradition of being described as neurogenic stuttering that should not respond to such fluency enhancements (Krishnan and Tiwari, Reference Krishnan and Tiwari2013). However, individuals with PD who stutter were found to respond to choral speech similar to individuals with developmental stuttering (Juste et al., Reference Juste, Sassi, Costa and de Andrade2018). Moreover, articulatory tools used in the therapy of neurodevelopmental stuttering, such as slowing speech rate as well as other articulatory techniques, can also help individuals with PD who stutter with their speech. These results require more studies about the common grounds for speech and other dysfluencies in PD and developmental stuttering.
The effect of auditory pacing in PD is more evident. Known as rhythmic auditory cueing (RAC), presenting a regular auditory stimulus such as a metronome or music with a salient beat improves significantly gait in PD patients (Fleming, Reference Fleming1942; Ghai et al., Reference Ghai, Ghai, Schmitz and Effenberg2018b; Kwakkel et al., Reference Kwakkel, de Goede and van Wegen2007). The intervention involves instructing patients to walk in synchrony with a regular sound or music with a distinct beat, often tailored to their preferred cadence (Benoit et al., Reference Benoit, Dalla Bella and Farrugia2014; Elston et al., Reference Elston, Honan, Powell, Gormley and Stein2010; Enzensberger et al., Reference Enzensberger, Oberländer and Stecker1997; Howe et al., Reference Howe, Lövgreen, Cody, Ashton and Oldham2003; McIntosh et al., Reference McIntosh, Brown, Rice and Thaut1997; Thaut et al., Reference Thaut, McIntosh and Rice1996). In the presence of a rhythmic stimulus, PD patients typically walk faster, increase their step length (McIntosh et al., Reference McIntosh, Brown, Rice and Thaut1997), and reduce the frequency of freezing episodes (Arias and Cudeiro, Reference Arias and Cudeiro2010). As in stuttering, this immediate effect tends to disappear after the end of the stimulation.
45.4.4 Shared Mechanisms
Both stuttering and PD share a common rhythmic component associated with difficulties in generating precise internal timing for motor actions, such as gait coordination and speech articulation. This rhythmic deficit involves inaccurate temporal predictions governing motor commands, resulting in disrupted movement initiation or execution. Interestingly, in both cases, the presence of an external rhythmic stimulus can alleviate these difficulties by compensating for the internal prediction inaccuracies. These observations support the characterization of stuttering and PD as motor-rhythm disorders. Both conditions involve alterations in the neuronal circuitry (subcortical-cortical network) underlying rhythm perception, production, and temporal prediction. Tasks involving beat perception and synchronization recruit similar neuronal circuitries, including the basal ganglia, premotor cortex, and pre-supplementary motor area (Chen et al., Reference Chen, Penhune and Zatorre2008; Coull et al., Reference Coull, Cheng and Meck2011; Dalla Bella et al., Reference Dalla Bella, Benoit and Farrugia2017; Grahn and Brett, Reference Grahn and Brett2007; Grahn and Rowe, Reference Grahn and Rowe2009; Repp, Reference Repp2005; Repp and Su, Reference Repp and Su2013; Schwartze and Kotz, Reference Schwartze and Kotz2013).
Another important aspect of rhythm deficits in both stuttering and PD is the role of automatization. In PD, neurodegeneration leads to de-automatization of movement, resulting, among other symptoms, in poorer dual-task performance. This aspect seems to be less evident in stuttering. However, Alm (Reference Alm2021) recently proposed that stuttering may involve less automatized speech sequences within the basal ganglia motor loop during childhood (see also Chang and Guenther, Reference Chang and Guenther2020). Stuttering symptoms would emerge during attempts to produce these poorly automatized sequences. De-automatization of speech production through the allocation of increased attentional resources, such as imitating others, speaking with an accent, or consciously altering speech rate and articulatory patterns, would then reduce stuttering. The effects of rhythmic fluency-enhancing conditions can be interpreted in a similar way, as strong beat-based rhythms provided by a metronome provide a temporal scaffolding supporting temporal predictions (Large and Jones, Reference Large and Jones1999; Schwartze and Kotz, Reference Schwartze and Kotz2013) capable of freeing up attentional resources.
45.5 Rhythm as a Viable Intervention for both PD and Stuttering
The aforementioned overlaps between PD and stuttering point to common deficits in temporal prediction and automatization. This suggests that (a) training temporal predictions for movement generation and (b) automatizing newly acquired timing patterns might have therapeutic potential for both classes of disorders. It is worth noting, however, that while both conditions are associated with rhythm and timing deficits, and their neural underpinning of these disorders partially overlap, there are significant differences. PD primarily involves degeneration in the dopaminergic pathways within the basal ganglia, impacting motor control and automatization. In contrast, stuttering is associated with deregulation of basal ganglia-cortical circuitries but is not accompanied by neurodegeneration, suggesting a more functional or developmental anomaly. Moreover, the role of the dopaminergic system in stuttering is not clear yet (Alm, Reference Alm2021). Therefore, while temporal prediction and rhythm training might benefit both classes of disorders by engaging common neural circuits including the basal ganglia and motor cortical areas, distinct functional mechanisms may be exploited in the two cases. For PD, rhythm-based therapies might aim to counteract or bypass dopaminergic deficits, whereas in stuttering, the focus could be on strengthening the functional connectivity and efficiency of the motor circuits involved. This distinction underscores the importance of tailored therapeutic interventions that, while exploiting the shared role of rhythm and timing, are also sensitive to the unique neural substrates of each disorder.
45.5.1 Training Exploiting Rhythmic Stimulation in PD
Several treatments are available to manage motor symptoms in PD. These include medication (such as levodopa and dopamine agonists) (Connolly and Lang, Reference Connolly and Lang2014), surgical procedures (such as pallidotomy or thalamotomy) (Lozano et al., Reference Lozano, Tam and Lozano2018), deep-brain stimulation (DBS) (Benabid et al., Reference Benabid, Pollak, Louveau, Henry and de Rougemont1987; Kalia et al., Reference Kalia, Sankar and Lozano2013), and noninvasive options such as physical therapy and neuromodulation techniques (transcranial magnetic stimulation or transcranial direct-current stimulation) (Benninger and Hallett, Reference Benninger and Hallett2015). Each treatment aims to compensate for dopamine loss or reduce the dysfunction in brain circuitries related to movement. In addition to pharmacotherapy and various other interventions, non-pharmacological treatments such as RAC are recognized for their beneficial effects in managing PD symptoms. These rhythm-based therapies complement traditional treatments and are increasingly acknowledged for their role in improving motor symptoms in PD patients. More generally, rhythmic stimuli have shown beneficial effects on motor behavior in patients with movement disorders and older adults (Ghai et al., Reference Ghai, Ghai and Effenberg2018a, Reference Ghai, Ghai, Schmitz and Effenberg2018b; Spaulding et al., Reference Spaulding, Barber and Colby2013). Most studies have focused on gait disorders due to their functional relevance, impact on quality of life, and economic burden. In the management of PD, where the effectiveness of dopamine replacement therapy diminishes over time (Grabli et al., Reference Grabli, Karachi and Welter2012; Sethi, Reference Sethi2008), there is a pressing need for innovative non-pharmacological approaches to improve gait. Rhythm-based interventions, such as walking to an auditory beat or participating in dance activities, hold promise in enhancing gait, quality of life, and social engagement among individuals with PD (for a review, see Dalla Bella, Reference Dalla Bella, Cuddy, Belleville and Moussard2020). These interventions leverage rhythmic auditory cues to provide a temporal framework that facilitates movement initiation and coordination (Ghai et al., Reference Ghai, Ghai, Schmitz and Effenberg2018b; Spaulding et al., Reference Spaulding, Barber and Colby2013).
RAC has an immediate beneficial effect on gait in PD (Arias and Cudeiro, Reference Arias and Cudeiro2010; Cochen De Cock et al., Reference Cochen De Cock, Dotov and Ihalainen2018; McIntosh et al., Reference McIntosh, Brown, Rice and Thaut1997). While these benefits tend to dissipate once the stimulation ceases, longer-term effects can be observed through RAC rehabilitation programs, as shown by Lim et al. (Reference Lim, van Wegen and de Goede2005). These programs involve regular RAC-assisted walking sessions, resulting in increased walking speed and reduced freezing phenomena at the end of the rehabilitation, even in the absence of stimulation (Dalla Bella et al., Reference Dalla Bella, Benoit and Farrugia2017; Nieuwboer, Reference Nieuwboer2008; Rochester et al., Reference Rochester, Burn, Woods, Godwin and Nieuwboer2009). Similar motor benefits are observed with home-based RAC rehabilitation using a stimulating device (Nieuwboer et al., Reference Nieuwboer, Kwakkel and Rochester2007). However, the long-term persistence of these effects and their interaction with neurodegenerative decline remain uncertain, with inconclusive evidence to date (Benoit et al., Reference Benoit, Dalla Bella and Farrugia2014; Marchese et al., Reference Marchese, Diverio, Zucchi, Lentino and Abbruzzese2000; Nieuwboer et al., Reference Nieuwboer, De Weerdt and Dom2001).
The exact nature of brain mechanisms underlying these beneficial effects still needs clarification. For example, the bases of RAC in PD is still a subject of ongoing debate (Dalla Bella et al., Reference Dalla Bella, Benoit, Farrugia, Schwartze and Kotz2015, Reference Dalla Bella, Dotov, Bardy and Cochen de Cock2018; Nombela et al., Reference Nombela, Hughes, Owen and Grahn2013; for a review, see Dalla Bella, Reference Dalla Bella, Cuddy, Belleville and Moussard2020). It is still unclear whether beneficial effects are mediated by spared brain mechanisms (cerebello-thalamo-cortical network) acting compensatorily, or by capitalizing on residual capacities of the impaired network in PD (basal ganglia-thalamo-cortical network). However, emerging evidence suggests that these mechanisms may extend beyond gait-specific processes and instead involve a more general-purpose network that supports rhythm perception, production, and temporal prediction (Dalla Bella, Reference Dalla Bella, Cuddy, Belleville and Moussard2020; Large and Jones, Reference Large and Jones1999; Piras and Coull, Reference Piras and Coull2011; Schwartze and Kotz, Reference Schwartze and Kotz2013). This idea is supported by studies indicating improved rhythm perception following RAC training (Benoit et al., Reference Benoit, Dalla Bella and Farrugia2014) and the observation that gait improvement through RAC is associated with individual rhythm perception and production abilities (Cochen De Cock et al., Reference Cochen De Cock, Dotov and Ihalainen2018; Dalla Bella et al., Reference Dalla Bella, Benoit and Farrugia2017, Reference Dalla Bella, Dotov, Bardy and Cochen de Cock2018). Notably, this hypothesis aligns well with the aforementioned general dysrhythmia hypothesis (Cantiniaux et al., Reference Cantiniaux, Vaugoyeau and Robert2010; Puyjarinet et al., Reference Puyjarinet, Bégel and Gény2019; Tolleson et al., Reference Tolleson, Dobolyi and Roman2015) and provides a coherent framework for understanding the broader implications of rhythm interventions.
A hypothesis arising from this theory posits that rhythmic training targeting a specific effector (e.g., hand, finger) may yield positive effects on motor control and rhythmic behavior in other effectors (e.g., oromotor, gait). This transfer effect could be facilitated by the shared mechanisms supporting temporal prediction (Dalla Bella, Reference Dalla Bella2022). To examine this hypothesis, we conducted a recent pilot study (Puyjarinet et al., Reference Puyjarinet, Bégel and Geny2022) involving patients with PD. During the study, participants underwent training using either a rhythmic tapping game (Rhythm Workers; Bégel et al., Reference Bégel, Seilles and Dalla Bella2018; Dauvergne et al., Reference Dauvergne, Bégel and Gény2018) or a nonrhythmic game (Tetris) over the course of one month. Both games were implemented as tablet apps. The rhythmic game required participants to tap along with various rhythmic auditory stimuli, with synchronization accuracy driving progress in the game. Remarkably, the rhythm intervention not only reduced motor variability in the trained motor domain (tapping) but also demonstrated a positive effect on an oromotor task (diadocokinesis task), unlike the control condition that showed no such effect. Moreover, these beneficial outcomes were correlated with improvements in rhythm perception. These promising findings provide evidence of transfer effects driven by rhythmic training in PD, and first causal evidence in support of the hypothesis of a general dysrhythmia in PD. If confirmed in further studies also involving other clinical populations, these findings might have particular significance from a clinical standpoint, whereby the effects of rhythmic training may extend from one effector and motor actions to others. This highlights the potential of rhythmic interventions as a valuable clinical tool for addressing motor impairments in various conditions, including developmental stuttering.
45.5.2 Potential of Rhythmic Training in Developmental Stuttering
Two decades ago, it was proposed that explicitly training the basal ganglia timing network may benefit rhythmic speech production in stuttering (Alm, Reference Alm2004; Fujii and Wan, Reference Fujii and Wan2014). However, to date, no therapeutic approach based on rhythmic pacing techniques has been established, as the effects tend to diminish immediately after the end of rhythmic stimulation. Some devices have been developed to mimic fluency-enhancing conditions, such as choral speech, during naturalistic speech interaction, with mixed results (e.g., Pollard et al., Reference Pollard, Ellis, Finan and Ramig2009). More recently, efforts have been focused on utilizing neuromodulation techniques to establish more efficient patterns of information flow in the brains of adults who stutter. For example, transcranial direct-current stimulation (tDCS), a technique through which brain regions are stimulated with very low electrical current during the execution of a task, was used in combination with rhythmic pacing, such as speaking with a metronome or choral speech, to enhance fluent speech production (Busan et al., Reference Busan, Moret, Masina, Del Ben and Campana2021). Although first results are promising, further research is needed to determine the potential and the exact conditions under which these techniques should be applied.
Further exploration could focus on investigating whether intense or long-term rhythmic training could serve as a naturalistic approach for individuals who stutter to enhance their temporal predictions. An initial step would involve assessing the relationship between musical training and the occurrence, severity, or therapy outcomes of stuttering. If individuals who stutter exhibit significantly lower levels of musical training compared to the general population, or if lower severity or therapy success is associated with musical or rhythmic abilities, this would provide a basis for examining the effects of musical and rhythmic training on stuttering. Currently, only a limited number of studies have investigated the relationship between music and stuttering, primarily regarding immediate fluency-inducing effects, with Falk (Reference Falk and Sammler2025) and Falk et al. (Reference Falk, Schreirer, Russo, Heydon, Fancourt and Cohen2018) providing comprehensive overviews. Secondly, it would be crucial to identify individual differences that distinguish which speakers who stutter would benefit from musical training versus those who would not. Lastly, research should assess whether general musical, nonverbal, or specifically verbal rhythmic training can produce transfer effects on self-paced everyday speech.
45.6 Summary
Stuttering and PD exhibit different etiologies, as well as notable clinical and age-related differences, which lead to classifying them as separate disorders. In spite of these differences, though, both disorders share a dysfunction in the basal ganglia-cortical circuitries that play a vital role in rhythm processing and temporal prediction. A pivotal notion in explaining this overlap is the concept of predictive timing, namely the ability to predict accurately the time of occurrence of an upcoming event (e.g., the next syllable, or the next step), based on the regular temporal structure of a sequence (Large and Jones, Reference Large and Jones1999; Piras and Coull, Reference Piras and Coull2011; Schwartze and Kotz, Reference Schwartze and Kotz2013). Our review examined the behavioral – clinical manifestations – and neuronal overlaps of stuttering and PD, underscoring that both conditions involve alterations in the neuronal circuitry (subcortical-cortical networks) underlying rhythm perception, production, and temporal prediction. For these reasons, we conclude that stuttering and PD can be classified as rhythmic-motor disorders, emphasizing the significance of rhythm in addition to motor dysfunction. This hypothesis has implications for novel intervention strategies exploiting shared neuronal circuitries underpinning temporal and rhythm processing, which could potentially benefit both stuttering and PD. While rhythm-based interventions such as RAC have been widely examined in PD, their efficacy in stuttering warrants further investigation. The emergence of new technologies, such as mobile devices and serious games, offers opportunities to implement rhythmic training protocols in a variety of populations, including developmental stuttering (Agres et al., Reference Agres, Schaefer and Volk2021; Dalla Bella, Reference Dalla Bella2022). These advancements provide a platform to test the effectiveness of rhythmic training in improving temporal prediction in both PD and stuttering.
45.7 Acknowledgements
Simone Dalla Bella is funded by a Discovery grant from the Natural Sciences and Engineering Research Council of Canada (NSERC), and by a Canada Research Chair in music auditory–motor skill learning and new technologies. Simone Falk is funded by a Discovery grant from NSERC, and by a Canada Research Chair in interdisciplinary studies on rhythm and language acquisition.
Summary
In this review, we compare rhythmic dimensions of stuttering and PD, two neurological conditions leading to dysfluencies and disruptions in motor control in speech and walking, respectively. The findings indicate common grounds in rhythm-related symptoms and neuronal resources, underscoring the relevance of rhythm for the classification of both disorders.
Implications
The chapter helps us to understand processes and neural resources underlying rhythmic alterations and temporal prediction in speech motor control and their links to gross motor function. The results will inform future research comparing speech and motor rhythms in different motor disorders including, but not limited to, speech and language disorders.
Gains
Based on the view that stuttering and PD are rhythmic-motor disorders, we can conceive new intervention strategies based on rhythm training. These rhythm-based interventions could motivate interdisciplinary research using new technologies and uniting scientists from the speech and language sciences as well as from cognitive (neuro)sciences.
Open access