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Parkinson’s
disease (PD) is a progressive, neurodegenerative disorder of the basal ganglia,
pathologized by the gradual dopaminergic deterioration of the nigrostriatal
pathway (ASHA, 2017; Pinto et al., 2004). The basal ganglia are a group of
nuclei with diffuse connections to the cortex, brainstem, and thalamus, which
collectively regulate the motor and premotor areas and allows for smooth,
volitional movements. The subcortical structure is also concomitant to pathways
that control autonomic motor function, procedural learning, routine behaviors,
cognition, and emotion— including the impaired pathway that projects from the
substantia nigra of the midbrain to the striatum of the basal ganglia. The
striatum, the largest nuclear complex of the basal ganglia, receives excitatory
input from regions of the cortex and basal ganglia, and both inhibitory and
excitatory input from the dopaminergic cells of the substantia nigra. These
cortical and nigral inputs to the striatum can project either directly or
indirectly to the globus pallidus, the primary output site of the basal ganglia
(Dickson, 2017). More specifically, the direct pathway results in increased
excitatory drive from the thalamus to the cortex, while the indirect pathway
via the subthalamic nucleus increases inhibition of the thalamic nuclei. Both
pathways regulate motor input to the thalamic nuclei, which project to the
primary and supplementary motor cortices.             

            Denervation of the indirect pathway,
certainly integral to the basal ganglia motor loop, manifests as both motor and
non-motor symptoms in individuals with PD. Occurring in the ventral lateral
substantia nigra, nearly 60-80% of dopamine-producing neurons are degenerated
before the motor symptoms of Parkinson’s are detected. The disease process of
PD primarily leads to neuromuscular dysfunction, which is characterized by rigidity,
tremor, bradykinesia, and postural instability (Dickson, 2017). These motor
impairments are demonstrated in hypokinetic or hyperkinetic behaviors such as immobility,
slow voluntary movements, resting tremors, increased muscle tone, disturbed
gait and posture, diminished facial expression, reduced range of motion,
slurred speech, and motor speech disorders. Typically, patients with PD exhibit
difficulty with speech, chewing, swallowing, and controlling saliva. Speech
disorders can occur in up to 89% of individuals with PD (Wertheimer et al.,
2014). In terms of non-motor symptoms, individuals can present with anomia,
impaired discourse comprehension, memory problems, confusion, executive dysfunction,
social withdrawal, and reduced quality of life (ASHA, 2017; Wertheimer et al., 2014).

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            Speech production is generated by the complex,
continuous coordination of the orofacial, laryngeal, and respiratory systems;
the speech process is thought to be a fine motor skill which must be regulated
in terms of sequence and duration with great accuracy, speed, and rhythmicity
(Gentil et al., 2003). Considering
speech requires the planning of articulatory movements in accordance with the
distributed networks of linguistic processes, the restricted muscular control
of speech-organs in individuals with PD result in a motor-speech disorder known
as dysarthria (Pinto et al., 2004). Dysarthria is associated with disturbances
in respiration, laryngeal function, airflow direction, and articulation
resulting in poor speech quality and intelligibility due to lack of
neuromuscular function (Enderby, 2013). This motor-speech impairment can also
be characterized by monotony of pitch and loudness, reduced stress, variable
rate, imprecise consonants, and a breathy, harsh voice. The features of
dysarthria are frequent symptoms of progressive neurological diseases, and have
a profound impact on the patient’s communication, and consequently his or her
relationships with friends and family.

            Oftentimes, speech therapy is used
to improve the range and consistency of sound production, intelligibility, and
communicative effectiveness of patients with dysarthria (Enderby, 2013).  Although therapy can be effective, subthalamic
nucleus deep brain stimulation (STN-DBS) is an alternative surgical treatment of
dopamine depletion for patients with PD that exhibit the previously described
motor complications (Takashi et al., 2017). The operation implants electrodes bilaterally
on the subthalamic nucleus, which are connected to a battery-powered pacemaker
that stimulates the abnormal axonal network. STN-DBS is thought to be effective
due to the STN’s optimal position in the excitatory basal ganglia circuit— the
stabilization of the feedback loop reduces tremor, slowness, rigidity,
dystonia, and dyskinesia (Gartner & Mandybur, 2016). However, altered
speech and language-related functions have been observed to be significant
side-effects of STN-DBS (Klostermann et al., 2011). This paper will explore the
biolinguistic effects of deep brain stimulation of the subthalamic nucleus on speech
and language processes in individuals with Parkinson’s Disease.

            While the beneficial effects of
STN-DBS on the primary motor impairments of PD are relatively well predictable,
changes in speech present variably across patients. It is widely accepted that
an exacerbation of dysarthria remains one of the most common side effects of
DBS therapy (Aldridge et al., 2016; Klostermann et al., 2011). Nevertheless,
due to its influence on the voice, respiratory, and articulatory subfunctions
of speech, the treatment is predominantly advantageous in these domains. Giving
credence to this claim, consistent improvements have been found for voice
tremor, rate of speech, and the ability to phonate vowels in a loud and
sustained manner. Klostermann et al. attribute these changes to the overall reduction
of the motor impairments that are evidenced at the level of speech—
acceleration of speech can be due to the antibradykinetic effects of DBS, and
improved phonation can be the result of a reduction of rigidity, which allows
for better control of respiratory and glottis function (2011). Similarly,
Hammer et al. contend that STN-DBS changes velopharyngeal control in patients
with PD (2011). In this study, 17 participants with PD were tested with
aerodynamic measures during syllable production with stimulation on, and again
1 hour after stimulation was off. The results found that the changes were
primarily consistent with a mild increase of intraoral pressure and
velopharyngeal closure in low frequency stimulation, two functions affected by
the motor symptoms of dysarthria. The findings also suggest that low frequency
stimulation is modestly correlated with measures of increased limb function,
however, DBS demonstrates a subtler influence on speech-related velopharyngeal
control than limb motor control. The authors also recognize that the
distinctions between speech and limb-related function in accordance with high
vs. low frequency are important to consider for the optimization of DBS
stimulation for individuals with PD (Hammer et al., 2011). Most seriously
strengthening the assertion that STN-DBS improves the manifestation of
dysarthria in individuals with PD is Gentil et al.’s (2003) study. The authors
establish that Parkinsonian symptoms are sensitive to STN stimulation,
evidenced by a 30-95% improvement in global motor abilities in patients during
DBS-STN. 

 The results found that participants under
stimulation presented a longer maximum phonation time, higher diadochokinetic rate,
greater stability of fundamental frequency in sentences, and lower fundamental
frequency during sustained vowels. To test these functions, the participants’
tongue and lip strength, as well as their acoustic signal, were assessed during
and after STN stimulation. Measured by the Unified Parkinson’s Disease Rating
Scale (UPDRS) III, the motor disabilities and consequent speech impairments of
all participants diminished with STN-DBS.  The UPDRS III measures faculties such as
speech, facial expression, resting tremor, acting tremor, rigidity, finger tap,
hand movement, rapid alternating movements, leg agility, rising from a chair,
gait, bradykinesia, and posture stability (Shahidi et al., 2017). The maximal
force of the three articulatory organs increased dramatically under
stimulation— 74% (upper lip), 93% (lower lip), and 66% (tongue)— and can be
attributed to a decrease in bradykinesia. Additionally, when compared to
unstimulated patients, stimulated individuals demonstrated a significantly
longer maximal phonation time of sustained vowels /a/ and /i/, improved
intonation contour of phrases, and faster repetitions of /pataka/ (Gentil et
al., 2003). These results indicate that STN stimulation successfully influences
the patients’ respiratory and laryngeal conditions by reducing rigidity of the cricothyroid
muscles.

            Disparate to Klostermann et al.
(2011), Hammer et al. (2011), and Gentil et al.’s (2003) contention for
favorable speech outcomes with STN-DBS, Xie et al. argue that even with motor
improvement, stimulation intervention has little to no effect on Parkinsonian
dysarthria (2011). Both with and without STN stimulation, 11 patients’ motor
abilities were evaluated using UPDRS III. Further, their acoustic signals were
recorded during the production of sustained vowels, repetitions of /pataka/,
and sentence production tasks. Of the five male and six female participants,
the respective UPDRS III scores demonstrated consistent improvement of motor
abilities with DBS on. However, there were limited changes in the patients’ speech
scores, evidenced by the instrumental analysis of their speech samples with and
without stimulation (Xie et al., 2011). It is worth noting that none of the
acoustic features of the participants’ speech worsened with STN-DBS. Two
possible explanations are proposed for the discrepancy between the improvement
of motor ability and invariable speech activity of the patients: speech may be
controlled by a pathway other than the aforementioned direct and indirect
avenues in the basal ganglia, or the five-point scale used in the UPDRS III is
not a sensitive enough tool to evaluate speech performance. The authors conclude
that regardless of speech abilities, the results support the perspective that
STN-DBS is an effective therapy method for the motor disabilities of
individuals with PD (Xie et al., 2011). In accordance with Xie et al.’s (2011)
findings, D’alatri et al.’s prior study maintains that while STN-DBS
significantly improved the participants’ motor performances, it provided no
functional improvement of their dysarthria (2006). The patients with PD were
assessed using the UPDRS III and a perceptual evaluation of speech with and
without DBS. An acoustic analysis of the speech samples (conversational,
reading task, diadochokinetic rate, sustained vowel) with stimulation switched on
did not reveal any deterioration or improvement in acoustic features. The
instrumental analysis also indicates that STN-DBS effects on speech were
limited to voice parameters as a result of stabilized glottal vibration.
Moreover, tremor indices showed an improvement of vocal tremor significantly
higher under stimulation than not. However, these parameters did not have any
substantial effect on speech intelligibility, prosody, and articulation,
therefore leading the authors to conclude that STN-DBS has no impact on speech
functionality in patients with dysarthria (D’alatri et al., 2006). While
STN-DBS is effective in treating the motor impairments that accompany
Parkinson’s disease, strong evidence does not exist to support the concurrent attenuation
of motor speech deficits.

            Although some evidence supports the positive
effects of STN-DBS on speech, Wertheimer et al. report that the treatment has
been associated with unfavorable impacts on intonation, rhythm, articulation,
and intelligibility (2014). To test this claim, the authors utilize a survey
method to examine the “patient’s perspective” of speech disturbances of both
DBS and non-DBS participants with PD. The Voice Handicap Index (VHI) is the
most standardized survey measure used to assess the psychosocial consequences
of a voice disorder by asking questions that correspond to self-perceptions of
voice characteristics, such as “My voice makes it difficult for people to hear
me,” or “My voice problem upsets me.” Within the younger participants (ages
50-69), the DBS group rated their speech difficulties to be more severe
compared to the non-DBS groups, reporting more difficulties with other people
understanding them, a greater reduction in overall communication, and less
socialization. Likewise, the older DBS group (ages 70+) rated numerous speech
difficulties as more severe compared to the non-DBS group. Independent of age,
the DBS participants’ VHI scores indicate a significantly higher impact
functionally, physically, and emotionally; with greater speech problems, more
severe disturbances, and a greater adverse impact of speech disturbances on
social interaction (Wertheimer et al., 2014). Further, in a study published in
the Iranian Journal of Neurology, authors Shahidi et al. explore the UPDRS
scores of Parkinson’s disease patients compared at pre-DBS operation, 6 months
and 6 years post-surgery, as a method to measure the long-term effectiveness of
DBS (2017). The procedure has demonstrated short-term improvements in motor
functions, but there is little evidence in support of STN-DBS improving long-term,
non-motor symptoms. The authors explain that DBS lessens the severity of motor
symptoms for a period of time, however, the relief from these symptoms is not
lasting.  In this cross-sectional study,
36 patients with advanced PD were evaluated with an UPDRS score before
undergoing STN-DBS surgery, and postoperative short-term (6 months) and long-term
(6 years) follow-ups were completed to compare UPDRS scores in each of the
patients. An analysis of these scores reveal significant differences between
preoperative scores and scores 6 years post-operation. Primarily, the worsening
of resting tremor, speech, rapid alternating movements of the hands, finger
tap, and facial expression were demonstrated by the participants. Generally,
total motor function decreased 6 years post-operation, in comparison to both
the preoperative and 6-month follow up scores. However, the authors found a
significant reduction in patients’ resting tremor in 6-year follow up scores compared
to their pre-operative state. Shahidi et al. suggest that STN-DBS causes the further
deterioration of the motor functions of the patient as an adverse effect of the
surgery, yet, the authors provide no evidence to support this claim (2017).

            Various approaches to studying the
impact of STN-DBS on linguistic models, including the assessment of language
under active versus inactive stimulation and before versus after the DBS
surgery, have been employed to track the effectiveness of the procedure on verbal
fluency, semantic priming, and prosody analysis in individuals with PD (Klostermann
et al., 2011). According to Klostermann et al., disordered language perception
and production based on basal ganglia, thalamic, or white matter damage are
viewed as the disruption of relay functions supporting cortical language
processing, rather than a dysfunction of the individual’s own linguistic operations
(2011). In a 2008 study, Boulenger et al. claim that the deprivation of striatal
dopamine in patients with PD eradicates the semantic priming of action words,
which is indicative of the selective engagement of motor networks in semantic
word perception. This suggests that semantically coded information is signaled
to the basal ganglia, which in turn executes language production. However, language
tasks were performed with electrode stimulation both on and off— patients with
PD had to decide if presentations of a word followed by a non-word contained
only real words or only non-words. The comparison of results of the groups’
performances infer that STN-DBS does not affect the automatic processes of
semantic access, evidenced by the decreased latency of responses with increased
semantic relatedness between the word pairs, and therefore weakening Boulenger
et al.’s (2008) assertion (Klostermann et al., 2011). Contrastively, Klostermann
et al. propose that STN-DBS primarily induces a decline in the verbal fluency,
of both letter and category type, of patients with PD (2011). In one cohort,
individuals with on-DBS were asked to produce as many word alliterations as
possible in a given time interval, independent of the semantic relationships between
the chosen words. In another control group, patients were asked to name as many
words denominating a specific category as possible. The results of both
language tasks imply that fluency in these conditions is significantly worse
than that in patients off-DBS (Klostermann et al., 2011). However, the authors acknowledge
that some verbal fluency deficits under DBS reflect global changes in cognitive
control due to the progression of PD, rather than an impact on primarily
linguistic processes. Further, STN-DBS has been found to have adverse effects
in prosody processing in patients with PD. The rostral portion of the
subthalamic nucleus is connected to the limbic system— a collection of
structures responsible for emotional regulation— and is thought to modulate the
perception of the emotional content of intonational language features. Changes
in prosody analysis in patients with PD can only be loosely tied to STN-DBS, considering
the basal ganglia are only candidate structures for decoding the dynamics of
language (Klostermann et al., 2011).  Overall,
STN-DBS appears to worsen the already weakened fluency and prosody processing
of patients with Parkinsonian dysarthria.  

            As evidenced in the diverse conclusions
made by these studies, the effects of STN-DBS on the speech and language
functions in patients with Parkinson’s disease are still widely uncharted. Although
the severity of the motor impairments caused by PD may be lessened with
stimulation therapy, its effects on speech and language are too variable to
claim that their deficits will too decline. The implications of this research
can be imperative for the treatment of Parkinson’s and the development of DBS
as a method to mediate symptoms. Primarily, patients should be educated about
the potential risks of DBS and have an understanding that the relief from motor
impairments is not long-term before undergoing the procedure. Patients should
also be prepared for further deterioration of their motor function to be
present after the effects of treatment wears off over the years. Finally, as
all studies acknowledge, the effects of STN-DBS on the motor impairments of patients
with PD need to be further researched to obtain a better understanding of the
treatment method. 

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