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DBS-STN and Speech: A Review of the Literature

The Parkinson Alliance/DBS-STN Research Team

Speech is a complex behavior that is coordinated by an integrated network of sensory, muscular, respiratory, and cognitive systems.

As a result of the complex nature of speech, symptoms of speech impairment can be quite diverse, reflecting dysfunction in one or more of these systems. Importantly, speech, which generally refers to articulatory and phonetic (i.e., speech sounds) aspects of verbal expression, is not the same thing as language, which refers more broadly to one's ability to comprehend, formulate, and express thoughts and feelings (Victor and Ropper, 2001).

Speech problems are common in Parkinson's disease (PD). For example, Harelius and Svensson (1994) found that 70% of persons with PD reported speech impairments after the onset of PD. The scientific literature examining speech in PD is vast and this "Current Science Review" is intended only as a summary of the literature relevant to DBS-STN. For a thorough review of speech difficulties in persons with PD, see Carter (1963, 1965a, 1965b) and Schulz & Grant (2000).

The clinical term used to generally describe speech problems in PD is hypokinetic dysarthria. Dysarthria refers to impaired articulation of speech. The term "hypokinetic" means diminished movement and decreased motor function. Thus, hypokinetic dysarthria refers to impaired articulation of speech as a result of decreased motor function. Characteristics of hypokinetic dysarthria include: monotonous and reduced pitch and loudness, variable rate of speech, short rushes of speech, imprecise consonants, and a breathy and harsh voice (Boshes, 1966; Canter, 1963, 1965a, 1965b; Sapir, 2001). In other words, the speech impairments can show themselves in PD through impacting vocal sounds, overall expression of words, breath control during speech, speech volume (softening speech volume), and/or prosody changes (i.e., changes in intonation or rhythm) of speech that reflect emotional expression (Pell & Leonard, 2003; Schulz & Grant, 2000).

Research examining the effect of DBS-STN on speech has utilized a variety of experimental designs, including assessments of speech before and after DBS-STN, comparisons of speech "on" versus "off" stimulation, comparisons of the effects of levodopa versus DBS-STN, comparisons of the effects of left vs. right STN stimulation, and individual case studies. In addition, research examining various treatments for speech dysfunction has been conducted. Below we summarize the essential findings of these research efforts. Studies comparing speech before and after DBS-STN have generally shown either no improvement or a decline in speech functioning following surgery. For example, Bejjani et al. (2000) examined the synergistic effects of levodopa and DBS-STN in 10 PD patients. Patients were assessed with the Unified Parkinson's Disease Rating Scale (UPDRS) before and six months after DBS-STN surgery.

The findings showed that speech was significantly improved by levodopa before surgery. However, additional improvement in speech beyond the improvement seen using levodopa alone before surgery was not seen following DBS-STN. Another study (Dromey et al., 2000) examined the effects of DBS-STN on acoustic measures of voice. Seven patients were assessed before and six-months after bilateral (i.e., both sides of the brain) DBS-STN. Speech was assessed both on and off medication during the pre and post-surgery evaluations. Two primary speech variables were assessed: fundamental frequency and speech intensity. Fundamental frequency corresponds to pitch and speech intensity corresponds to the perception of how weak or strong a person's voice is.

The results found only modest improvements in speech functioning and, according to the authors, "the overall impact is not substantial and would not represent a functionally useful change in speech performance." The authors noted that the patient's speech was only mildly impaired before surgery and therefore improvement may have been difficult to detect. Krause et al. (2004) examined the effects of DBS-STN in 27 patients. Patients were assessed with the UPDRS before and yearly after surgery. The average follow-up time was 29.8 months (about 2 years). Data were reported for changes in UPDRS scores in four conditions: off-meds/off-stimulation, on-meds/off stimulation, off-meds/on stimulation, on-meds/on stimulation. Consistent with other studies, significant improvement in motor functioning was seen in most patients. The UPDRS has one item that assesses speech. In this sample, after surgery and when on-medication, speech was improved. However, when off-meds and on stimulation, speech actually worsened. Another study has found that DBS-STN can have deleterious effects on speech production. Thobois and colleagues (2002) examined eighteen consecutive severely affected PD patients before and 6 months after the DBS-STN.

Although this study confirms the great value of subthalamic nucleus stimulation on the non-speech motor symptoms of PD, the investigators found that DBS-STN adversely affected speech production in one of their participants. Krack et al. (2003) examined the long-term (i.e., 5 year) outcome of bilateral DBS-STN in 49 PD patients. Patients were assessed on and off medication. The UPDRS, as well as neuropsychological tests, were administered at one, three, and five years after surgery. The results at five-years showed 54% improvement in UPDRS motor scores when off medication. However, speech functioning declined in these patients after five-years. This result was interpreted as a reflection of the expected decline in speech that one would see in DBS-STN treated patients.

According to this study, DBS-STN does not appear to confer any protection against declines in speech functioning in the long-term. In contrast to the studies described above, a series of studies conducted by Gentil and colleagues have found subtle improvements in motor control of the lips and tongue, acoustic features of speech, and articulatory control. For example, Gentil et al. (1999) examined oral control in 10 patients with DBS-STN compared to 14 normal control subjects. Patients were assessed with the UPDRS and a device that measures compression forces of the lips and tongue. Compared to the off-stimulation condition, the speech item from the UPDRS improved when stimulation was on, although for only one patient was their speech described as normal. Stimulation resulted in a near-normalization of other motoric-speech variables, such as the force of lip and tongue movements and of oral-reaction time.

These findings were replicated in another study (Gentil et al., 2003). Pinto et al. (2003) examined speech production in detail in 16 PD patients on and off bilateral DBS-STN stimulation. The patients' speech was moderately impaired when assessed without medication and without stimulation. Speech production was quantitatively assessed by measuring the force of the lips and tongue and the acoustic features (i.e., duration, vocal vibration, intensity) of vocal expression. The results showed that on stimulation, patients showed a large increase in maximal force of the lips and tongue. In addition, a reduction in speech pauses and an increase in phonemic length were observed during stimulation. In another study (Gentil et al., 2001) the acoustic parameters of speech (including phonemic duration, fundamental frequency, and relative intensity) in various speech tasks in 26 PD patients were examined while on or off stimulation. The patients' speech was moderately impaired when assessed without medication and without stimulation. The results showed that while on stimulation, patients were able to lengthen their maximal phonation time of sustained vowels and reduced their pauses in phrase repetitions during a 30 second speech sample. During STN stimulation, patients varied their intonation more and their speech sounded more normal and natural. Speech intensity, which reflects the strength of phonation (e.g., weakness of voice), was not affected. Taken together, these studies indicated that some improvement occurs in the motoric and acoustic components of speech during stimulation, but the authors noted that the results are not applicable to patients with more severe speech disorders. In addition, the changes observed using sensitive measures of motor force and changes in voice acoustics may not translate into clinically significant (i.e., readily observable or meaningful on a day-to-day basis) improvements. Lateralization studies (studies examining the functions of the right and left hemispheres of the brain) are also contributing to our understanding the impact of DBS-STN on speech. Before discussing studies that address lateralization and speech, it is important to explicate speech function as it pertains to hemispheric function in the brain. Speech is a bilateral motor activity controlled mainly by the left hemisphere (Devinsky & D'Esposito, 2004). In other words, although language functions are involved in both sides of the brain, the left hemisphere mainly controls speech output in the majority of people. Moreover, Kolb and Whishaw (2001) indicated that the left hemisphere generally plays the most important role in speech production, while the right hemisphere plays a larger role in auditory comprehension. Of note, for 96 percent of right-handed individuals, speech is controlled by the left hemisphere, leaving 4 percent of right-handed individuals having a right-hemispheric dominance. In contrast, for 70 percent of left-handed individuals, speech is dominant in the left hemisphere; for 15 percent speech is dominant in the right hemisphere, and for 15 percent it is controlled by both hemispheres (Devinsky & D'Esposito, 2004; Rasmussen & Milner, 1977).

There are interesting implications to this information in the context of DBS-STN, which are only speculative at this point in time. For individuals with DBS in the left hemisphere, there is increased likelihood of changes in speech. Conversely, if one has right-sided DBS the changes in speech may be less severe, if there are any changes at all. Of course, this all depends on where the dominant function of speech is in an individual. One needs to keep in mind, however, speech changes occur in a large amount of PD patients with and without DBS, as speech anomalies have been reported to be quite common in the progression of PD. The lateralization effects of DBS-STN on speech are illustrated in the following studies. Santens and colleagues (2003) found lateralized effects of STN stimulation on different aspects of speech in Parkinson's disease. Specifically, this study is the first to examine laterality effects (the effects of right and left stimulation) on speech characteristics in patients with bilateral DBS-STN. Seven patients who had bilateral stimulation were examined.

First, the seven patients were asked to read a 200-word standard passage, and then they were asked to perform sustained vowel "ah" phonation. The two tasks were performed in four different conditions of STN stimulation: (1) left on, right off; (2) right on, left off; (3) bilateral stimulation off; and (4) bilateral stimulation on. Significant differences were found between left and right stimulation. Santens and the co-investigators found that right STN stimulation did not have an effect on speech when compared to bilateral stimulation "off," irrespective of the status of the left-sided stimulation. However, when left-sided stimulation is "on," this stimulation negatively influences speech when right-sided stimulation is "off." They found that these effects coincided with the subjective impressions of the different stimulation conditions by the patients themselves.

The investigators concluded that selective left-sided stimulation has a profoundly negative effect on prosody, articulation, and intelligibility. Right-sided stimulation did not display this side effect. There is no significant difference in speech characteristics between bilateral stimulation on and off. The investigators suggest that a balanced tuning of bilateral basal ganglia networks is necessary for speech, and that the left circuit is probably dominant. Furthermore, it is not inconceivable that left-sided STN stimulation might differentially alter speech when compared to right-hemisphere stimulation when considering that the functional anatomic representation of speech is in the left-hemisphere for the majority of individuals, as previously mentioned. The researchers conclude that bilateral tuning is of great import and will likely help manage the deleterious effect that STN stimulation may have on speech.

Another study examined the effect of unilateral electrostimulation of the STN on different speech subsystems in six, right-handed patients with PD (Wang et al., 2002). Three of the patients received the implantation of the deep brain stimulator in the right STN, and three received the stimulation in the left STN. Speech recordings were made in the medication-off state at baseline, and at three moths post surgery with stimulation "on" and with stimulation "off." Results showed that all six participants demonstrated improvement on the Unified Parkinson's Disease Rating Scale (UPDRS-III) - improvement on all non-speech motor tasks. However, there were interesting findings with regard to the impact of unilateral stimulation on speech functions. There was an appreciable, albeit mild, improvement on the respiratory/phonatory subsystems for those receiving right-sided DBS-STN. In contrast, the three subjects who received left-STN stimulation showed a significant decline in vocal intensity and vowel duration from their baseline. In other words, in this study when the DBS-STN is in the left-hemisphere for right-handed individuals (likely the dominant hemisphere where speech production is controlled), worsening of speech resulted.

The authors concluded that speech function is very susceptible to micro lesions due to the surgical procedure itself when the surgical site was in the dominant hemisphere of the brain. There are also a couple of case studies that examine the effects of DBS-STN on speech function. One study examined the effects of DBS-STN on voice and speech characteristics in one male PD patient (Hoffman-Ruddy et al, 2001).

The study concluded that DBS-STN had positive effects in the voice and speech measures utilized, which was indicative of increased support and coordination of multiple speech and voice subsystems (respiration, phonation, articulation, resonance, and prosody). The authors purported that a decrease in rigidity and bradykinesia can positively impact respiratory and laryngeal preparation for speech production. Furthermore, they found that increased speech intensity levels, pitch range, and acoustic measures directly correlated to the amount of subglottal pressure generation (pressure between the thin strips of muscle inside the throat that produce sound by moving slightly as air travels over them) and laryngeal muscle coordination. They cautioned the reader about generalizability, as this study only had a sample size of one. A case illustration was provided by Moretti and colleagues (2003), which demonstrated "speech initiation hesitation" following STN stimulation. The individual who underwent surgery was a 68 year-old man with a 14-year history of PD and severe rigidity, severe akinesia, gait freezing, and moderate tremor while resting. This individual manifested speech initiation hesitation but no other motor symptoms after DBS-STN. The researchers found that one-month after his surgery, he reported difficulty in initiating speech. Initial stuttering was very limiting for the patient who began a word 3 to 4 times, repeating the first phoneme or the initial syllable. The hesitation was not correlated with the "freezing" of speech (the brief inability to produce speech due to impaired muscular control). Automatic speech was conserved, and he did not have difficulties reading or writing. These investigators conclude that chronic simulation may help to restore the language control of the deep brain circuits or it may implement the prefrontal cortex [of the brain]. The result may be consistent with a slowness of cognitive activity and a reduction of the amount of words produced. Finally, it is worthwhile to comment on some studies that examined treatment for speech anomalies in patients with PD. Schulz and Grant (2000) conducted a review of the different treatment approaches for persons with PD up to the time of their manuscript and examined the effects of these treatments on speech. Treatment methods reviewed include speech therapy, pharmacological, and surgical. Their review showed that speech therapy (when persons with PD are optimally medicated) has proven to be the most efficacious therapeutic method for improving voice and speech function. Therapeutic devices have included the voice amplifier, delayed auditory feedback (DAF), the wearable intensity biofeedback device, and a masking device. The authors' review stated that pharmacological methods of treatment in isolation do not appear to significantly improve voice and speech function in PD across recent research studies. Surgical treatment methods including pallidotomy and deep brain stimulation may be significant treatment options, which improve voice and speech function in some persons with PD; but they indicated that more research needs to be conducted before determining its effects in this domain. In sum, they found that speech therapy is the most effective method in improving voice and speech production in persons with PD. Since the aforementioned study was conducted, the literature reports that the impact of medicinal treatment of dysarthria is controversial and surgery, in general, appears to worsen the problem. Consequently, more and more research is examining the benefits of speech therapy for individuals with PD. de Swart and colleagues (2003) found that the utilization of the Pitch Limiting Voice Treatment (PLVT) increased loudness and at the same time sets vocal pitch at a better level. The authors argue that that an approach focusing solely on an increase of phonatory-respiratory effort has adverse effects because it raises vocal pitch and laryngeal muscle tension. However, their treatment produced an increase in loudness, while limiting an increase in vocal pitch and preventing a strained or pressed voice, which can cause dysarthria. Lastly, there have been several studies examining the benefits of the Lee Silverman Voice Treatment (LSVT), a behavioral treatment program for speech abnormalities. In general, LSVT seemingly improves many aspects of speech production. Sharkawi and colleagues (2002) studied eight patients with idiopathic Parkinson's disease and found the LSVT method to help with the neuromuscular control of the entire upper aerodigestive tract, which improved vocal intensity as well as oral tongue and tongue base function during the oral and pharyngeal phases of swallowing. Cabrejo and co-investigators (2003) strongly recommend the LSVT, indicating that this phonation re-education method has proven to be beneficial. Furthermore, Ramig and colleagues (2004) presented the essential concepts and outcome data for the Lee Silverman Voice Treatment, and the research has yielded significant long-term improvement in speech and voice functions in individuals with idiopathic Parkinson's disease In conclusion, the evolutionary aspects of studying speech disruption in PD have lead to tremendous advances in methodological approaches, and there have been numerous investigations examining the effect of DBS-STN on speech functions with these sound approaches. Although some research has found speech to be improved by bilateral DBS-STN (Gentil et al. 2003; Hoffman-Ruddy et al, 2001), the majority has suggested that the increase of impaired speech might be an underestimated problem in this population (Cabrejo et al., 2003; Dromey et al., 2000; Gentil, 1999; Santens et. al., 2003; Wang et al., 2002). There is convincing evidence that STN stimulation can have either no impact on the natural progression of speech problems in PD, or it may have a deleterious effect on speech. Of growing interest is the impact of DBS-STN on speech in relation to lateralized functions of the brain. For example, studies have found that in the majority of individuals left-sided STN stimulation might differentially alter speech when compared to right-hemisphere stimulation. Moreover, more and more research is finding that dysarthria, if not the exacerbation of, is a potential side effect of STN stimulation. In fact, some patients have described their speech problems as being the most debilitating of PD symptoms, even after DBS-STN. Of course, more research including larger samples, longitudinal examination, and sound methodology needs to be conducted to assess, verify, and provide further insight into the impact of DBS-STN on speech.

Future research will hopefully help us more fully understand what patient and treatment factors influence speech after DBS-STN. We will continue to monitor this area of research and update this review upon the publication of further studies.

References
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