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Speech production in Parkinson’s disease: neuroimaging findings
Serge Pinto
Laboratoire Parole et Langage, CNRS UMR6057, Aix-en-Provence
serge.pinto@lpl.univ-aix.fr
Introduction
Dysarthric speech is one of the frequent signs of Parkinson's disease (PD), which appears
generally in the later stage of the disease. The description of Parkinsonian dysarthria is
classically a ″monotony of pitch, monotony of loudness, reduced stress, short phrases, variable
rate, short rushes of speech, and imprecise consonants″ (Darley et al., 1975). These
characteristics have been attributed to the weakness and slowness of movement (referred
respectively as hypokinesia and bradykinesia), rigidity and tremor at rest. Any or all components
of speech production may be affected, including alterations of the respiratory, phonatory and
articulatory systems. The progressive dopaminergic cell loss of the nigro-striatal pathway,
projecting from the substantia nigra pars compacta to the striatum, is the main cerebral lesion
and notably, the origin of the motor loop dysfunction involving the basal ganglia (Alexander et
al.
, 1990). This denervation leads to the appearance of Parkinsonian motor symptoms among
which is the alteration of speech.
Cerebral activations associated with motor tasks in Parkinson’s disease
Recent findings revealed that dysfunctions observed during motor speech tasks do not parallel
those associated with limb movements.
Upper limb movements - During the execution of a manual, freely chosen, unilateral motor task,
underactivation (i.e a reduction of regional cerebral blood flow) was found in the supplementary
motor area (SMA), dorsolateral prefrontal (DLPFC) and anterior cingulate cortices of PD
patients compared to normal subjects (Playford et al., 1992). These cerebral areas are
respectively the main output projections of the basal ganglia to the motor, associative and limbic
loops. Conversely, the primary motor (M1), parietal and lateral premotor cortices were normally
activated. Studies have demonstrated an overactivation involving, among others, the lateral
cerebellum-parietal-premotor cortex circuitry (Samuel et al., 1997), as potentially a
compensation for the decreased activation of the basal ganglia motor loop. M1 cortex, both ipsi-
and contralateral to the limb movement, may also be overactivated in PD even in early stages of
the disease (Sabatini et al., 2000). These abnormal activation patterns depend obviously on the
nature of the task: during an externally-cued, sequential and repetitive motor task, the SMA is
normally activated in PD while the M1 cortex and the cerebellum are underactivated (Turner et
al.
, 2003). All these data together represent the commonly accepted background that
characterises PD cerebral dysfunctions associated with (proximal) limb movements.
Speech movements - Liotti et al. (2003) showed that abnormalities of brain activation associated
with PD speech were essentially represented by an overactivation of orofacial M1 cortex,
inferior lateral premotor cortex and SMA. Another study showed that in PD, there is 1/ a lack of
activation in the right orofacial M1 cortex and bilateral cerebellar hemispheres, 2/ an abnormal
increased of haemodynamic response in the right superior premotor cortex and bilateral
dorsolateral prefrontal cortex (DLPFC), and 3/ an overactivation of the SMA (Pinto et al.,
2004a). The authors suggested that Parkinsonian dysarthria is associated with an altered
recruitment of the principal brain motor regions (orofacial M1 cortex, cerebellum), and an
increased involvement of premotor and prefrontal cortices (DLPFC, SMA, superior premotor
cortex). This would represent either a compensatory phenomenon or the inherent activation
pattern underlying brain dysfunctions of PD dysarthria. In both studies, the activation patterns
dids not parallel those associated with hand motor tasks and may explain the frequent
therapeutical challenge encountered by the clinician who has to deal with the heterogenous
responses of limb and speech movements to pharmacological and surgical therapies.
Furthermore, evolution of the disease along time is concomitant with aggravation of dysarthria,which suggests that it is also linked to the increasing severity of cerebral non-dopaminergiclesions. Thus, PD dysarthria physiopathology cannot be restricted to the alteration of the motorbasal ganglia loop: the cerebellum-M1 cortex circuitry may also play a key-role in theappearance of dysarthric spech in PD.
Towards a better understanding of PD dysarthria physiopathology: what should we learn
from the deep brain stimulation experience
Improvement of individual speech parameters (Dromey et al., 2000 ; Gentil et al., 2001 ; Pinto et
al.
, 2003) following stimulation of the subthalamic nucleus (STN), which is recognised as one of
the most efficient surgical treatment for Parkinsonian signs, is often not sufficient to achieve
substantial improvement of speech intelligibility (Rousseaux et al., 2004 ; Törnqvist et al.,
2005). Motor control of the overall anatomo-functional system underlying speech production, i.e.
the pneumo-laryngo-articulatory coordination, does not seem to be sensitive to the modification
of neuronal activity within the basal ganglia and subthalamic areas induced by the surgical
procedure. Apart from the interpretation we already addressed in terms of implication of the
cerebello-cortical circuitry involvement, the current spread towards fibres of the cortico-bulbar
tract, which innervates essentially the orofacial musculature, has to be also taken into account.
This concept also includes other neighbouring structures that should not be concerned by the
chronic electrical stimulation around the STN: thalamus, cerebello-thalamic fibres or even
substantia nigra pars reticulata, Inadequate stimulation parameters or localisation represent
issues that have to be dealt with to ensure the optimal stimulation adjustment (Pinto et al., 2005).
Conclusions
So far, only two positron emission tomography (PET) studies are available in regards to the
cerebral activations associated with Parkinsonian dysarthria. Even if important issues have been
addressed, it is still difficult to conclude on the cerebral changes related to PD dysarthria, still
precluding PD dysarthria management by the clinician and its acceptance by the patient. In this
context, neuroimaging is a useful and promising technique able to further our knowledge
regarding dysarthria, particular and highly disabling sign among PD motor signs.
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