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					                                               Journal of Motor Behavior, Vol. 41, No. 6, 2009
                                                   Copyright C 2009 Heldref Publications


Proprioception and Motor Control in Parkinson’s Disease
Jurgen Konczak1,6, Daniel M. Corcos2, Fay Horak3, Howard Poizner4, Mark Shapiro5, Paul Tuite6, Jens
 ¨
Volkmann7, Matthias Maschke8
1
 School of Kinesiology, University of Minnesota, Minneapolis. 2Department of Kinesiology and Nutrition, University of Illinois
at Chicago. 3Department of Science and Engineering, Oregon Health and Science University, Portland. 4Institute for Neural
Computation, University of California–San Diego. 5Department of Physical Medicine and Rehabilitation, Northwestern
University, Chicago, Illinois. 6Department of Neurology, University of Minnesota, Minneapolis. 7Department of Neurology,
Universitat Kiel, Germany. 8Department of Neurology, Bruderkrankenhaus, Trier, Germany.
         ¨                                                ¨


ABSTRACT. Parkinson’s disease (PD) is a neurodegenerative dis-               cles, tendons, and joint capsules. These receptors provide
order that leads to a progressive decline in motor function. Growing         information about muscle length, contractile speed, muscle
evidence indicates that PD patients also experience an array of              tension, and joint position. Collectively, this latter informa-
sensory problems that negatively impact motor function. This is es-
pecially true for proprioceptive deficits, which profoundly degrade           tion is also referred to as proprioception or muscle sense.
motor performance. This review specifically address the relation              According to the classical definition by Goldscheider (1898)
between proprioception and motor impairments in PD. It is struc-             the four properties of the muscle sense are (a) passive mo-
tured around 4 themes: (a) It examines whether the sensitivity of            tion sense, (b) active motion sense, (c) limb position sense,
kinaesthetic perception, which is based on proprioceptive inputs, is         and (d) the sense of heaviness. Alternatively, some use the
actually altered in PD. (b) It discusses whether failed processes of
proprioceptive-motor integration are central to the motor problems           term proprioception to indicate the limb position sense and
in PD. (c) It presents recent findings focusing on the link between           kinaesthesia to refer to limb motion sense (Gardner, Mar-
the proprioception and the balance problems in PD. And (d) it dis-           tin, & Jessell, 2000), a definition we do not adopt. Within
cusses the current state of knowledge of how levodopa medication             the framework of this review, we use the term kinaesthesia
and deep brain stimulation affect proprioceptive and motor func-             to refer to the conscious perception of limb and body mo-
tion in PD. The authors conclude that a failure to evaluate and to
map proprioceptive information onto voluntary and reflexive motor             tion. We use the term proprioception to refer to the uncon-
commands is an integral part of the observed motor symptoms in               scious processing of proprioceptive signals used for reflexive
PD.                                                                          and postural motor control while recognizing that proprio-
                                                                             ceptive information also forms the basis for kinaesthesia.
Keywords: basal ganglia, kinaesthesia, movement disorder, senso-
rimotor integration                                                          The importance of proprioception for motor function such
                                                                             as reaching and grasping, static balance, and locomotion has
                                                                             been well documented (Butler et al., 2004; Diener, Dichgans,
                                                                             Guschlbauer, & Mau, 1984; Dietz, 2002; Sainburg, Ghilardi,
      ovement abnormalities such as tremor, bradykinesia,
M     rigidity, and postural problems constitute the clinical
hallmarks of Parkinson’s disease (PD). They are thought to
                                                                             Poizner, & Ghez, 1995). Patients with a loss of proprioception
                                                                             are still able to execute motor tasks, yet their motor behav-
                                                                             ior is gravely compromised. Goal-directed movements lack
arise primarily from the loss of dopamine producing neurons                  precision and postural and spinal reflexes are altered leading
and subsequent dysfunction of the basal ganglia-thalamo-                     to problems with balance and gait (Dietz; Ghez, Gordon, &
cortical pathway. Yet, a growing body of research demon-                     Ghilardi, 1995; Rothwell et al., 1982).
strates that PD also is associated with an array of perceptual                  It is the purpose of this review to summarize the current
deficits, such as odor and tactile discrimination and detec-                  knowledge of the extent of kinaesthetic deficits in PD. The
tion (Herting, Schulze, Reichmann, Haehner, & Hummel,                        review is guided and structured around four main questions:
2008; Mesholam, Moberg, Mahr, & Doty, 1998; Pr¨ torius,a                     First, is there evidence that kinaesthetic sensitivity is altered
Kimmeskamp, & Milani, 2003; Sathian, Zangaladze, Green,                      in PD? Second, are the motor problems in PD the result of
Vitek, & DeLong, 1997; Zia, Cody, & O’Boyle, 2003),                          failed processes of proprioceptive-motor integration? Third,
weight and pain perception (Maschke, Tuite, Krawczewski,                     what is the link between the proprioception and the balance
Pickett, & Konczak, 2006; Nolano et al., 2008), or the per-                  problems in PD? And fourth, how does levodopa medication
ception of visual depth (Maschke, Gomez, Tuite, Pickett, &                   and deep brain stimulation (DBS) affect proprioceptive and
Konczak, 2006). Recent evidence suggests that kinaesthesia                   motor function in PD? Before addressing these four ques-
is especially affected by PD and that such loss of kinaesthetic              tions, we briefly review neurophysiological evidence that
sensitivity is closely linked to the motor deficits (Adamovich,               links proprioceptive function to neural processes in the basal
Berkinblit, Hening, Sage, & Poizner, 2001; Contreras-Vidal
& Gold, 2004; Demirci, Grill, McShane, & Hallett, 1997;
O’Suilleabhain, Bullard, & Dewey, 2001).
                                                                                                          u
                                                                                Correspondence address: J¨ rgen Konczak, Human Sensorimo-
   Kinaesthesia is commonly defined as the conscious aware-                   tor Control Laboratory, School of Kinesiology, University of Min-
ness of body or limb position and motion in space. It is based               nesota, 1900 University Ave. SE, Minneapolis, MN 55455, USA.
on sensory information derived from receptors in the mus-                    e-mail: jkonczak@umn.edu


                                                                       543
J. Konczak et al.

ganglia and describe how the neural output of the basal gan-
glia is altered by PD.


        Proprioception and the Basal Ganglia
   Animal studies have long established that many basal gan-
glia neurons have proprioceptive receptive fields, responding
both to passive and active joint motions (Crutcher & DeLong,
1984a, 1984bb; DeLong, Crutcher, & Georgopoulos, 1985).
In humans, single cell recordings in PD patients submitted
to neurosurgery revealed that a third of the neurons in the
nucleus subthalamicus responded to passive or active move-
ments of limbs, the oromandibular region, or the abdominal
wall (Rodriguez-Oroz et al., 2001). These neuronal responses
are joint specific with several reports showing that the vast
majority of neurons in the monkey globus pallidus internal           FIGURE 1. The basal ganglia-thalamocortical circuitry.
(GPi) respond to passive motion of a single joint (Boraud,           Degeneration of the nigrostraital dopamine pathway (SNc
                                                                     → Striatum) leads changes in the two striato-pallidal pro-
Bezard, Bioulac, & Gross, 2000; Filion, Tremblay, & Bedard,          jections (direct and indirect pathways). STN = nucleus sub-
1988). However, when these monkeys were made parkinso-               thalamicus; SNr = substantia nigra, pars reticulata; SNc =
nian through 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine            substantia nigra, pars compacta; GPe = globus pallidus ex-
(MPTP) treatment, the number of cells responding to passive          ternus; GPi = globus pallidus internus; PPN = pedunculo-
movement increased, with most neurons now responding to              pontine nucleus.
movements of several joints. Researchers also observed this
loss in neuronal response specificity in the efferent projec-
tions of the basal ganglia to the thalamus (Pessiglione et al.,   synchronization means a reduced responsiveness to signals
2005) and supplementary motor area (Escola et al., 2002).         related to a particular context or action. In addition, the out-
Therefore, this disturbance of neural function is propagated      put may lose topographic specificity (Bergman et al., 1998).
throughout the striato-pallido-thalamo-cortical system. For       In information processing terms, this implies that the signal
example, in intact monkeys, thalamic neurons receiving basal      to noise ratio of basal ganglia neural processing is altered
ganglia afferents mostly respond to movement around a sin-        in parkinsonism (Bar-Gad & Bergman, 2001). Such an in-
gle joint. Following MPTP-induced parkinsonism, the tuning        crease in neural noise in the basal ganglia likely impairs the
of the proprioceptive receptive fields of these thalamic neu-      facilitation and modulation of premotor regions that must act
rons was markedly broadened thus providing much noisier           synergistically to generate accurate and well-timed move-
and less differentiated proprioceptive information to cortical    ment (Graybiel, 1998, 2005; Leiguarda et al., 2000).
motor regions.
   In general, the neurodegenerative processes associated
                                                                          Altered Kinaesthetic Sensitivity in PD
with PD may lead to abnormal neural hyper- or hypoac-
tivity in the basal ganglia and could act as a constant facil-       Although routine clinical examination often fails to
itator or brake on its efferent target structures (Pessiglione    demonstrate sensory changes, sensory alterations have been
et al., 2005). The classical view regards an imbalance be-        documented in PD (Snider, Fahn, Isgreen, & Cote, 1976).
tween the direct and indirect pathways projecting from the        Early reports showed that approximately 40% of PD patients
striatum to the globus pallidus internus/substantia nigra pars    experience spontaneous abnormal sensations despite having
reticulata (GPi/SNr) as the major cause of the increased fir-      a normal neurological examination (Koller, 1984).
ing rate in GPi/SNr (DeLong, 1990). This increased firing             Neurophysiological studies have demonstrated that pa-
inhibits thalamic projections to cortical motor areas thus re-    tients with Parkinson’s or Huntington’s disease show severely
ducing motor cortex excitation (see Figure 1). The reduced        depressed frontal somatosensory-evoked or proprioception-
activation of motor cortical neurons is then believed to be       related potentials (Abbruzzese & Berardelli, 2003; Rossini,
responsible for the observed bradykinesia, the patients’ in-      Filippi, & Vernieri, 1998; Seiss, Praamstra, Hesse, &
ability to activate a selected motor program or their failure     Rickards, 2003). Behavioral studies have suggested that basal
to inhibit competing motor programs (Mink, 1996). A more          ganglia dysfunction leads to an altered sensitivity of arm po-
recent, alternative view is that basal ganglia neurons become     sition sense (Klockgether, Borutta, Rapp, Spieker, & Dich-
excessively synchronized at low frequencies in PD and the         gans, 1995; Schneider, Diamond, & Markham, 1987; Zia,
MPTP model of PD (Bevan, Magill, Terman, Bolam, & Wil-            Cody, & O’Boyle, 2000, 2002). However, it has remained
son, 2002; Gatev, Darbin, & Wichmann, 2006; Goldberg,             unclear whether these findings were solely because of im-
Rokni, Boraud, Vaadia, & Bergman, 2004; Raz et al., 2001;         paired kinaesthesia or could be attributed to problems in vi-
Raz, Vaadia, & Bergman, 2000). This excessive neuronal            sual and cognitive processing; both of which are known to be

544                                                                                                    Journal of Motor Behavior
                                                                       Proprioception and Motor Control in Parkinson’s Disease

impaired in PD (Antal, Bandini, Keri, & Bodis-Wollner,              detecting changes in limb position sense is reduced at distal
1998; Diederich, Raman, Leurgans, & Goetz, 2002). In ad-            and proximal arm joints in PD.
dition, the possibility needs to be excluded that kinaesthetic         The previously mentioned studies have established that PD
deficits are simply the result of the known motor deficits of         patients have difficulties detecting or determining limb posi-
PD or are caused by some compensatory motor strategy.               tions. Another important aspect of kinaesthesia is the ability
   Recently, researchers in several psychophysical studies at-      to sense limb motion. Researchers still have an incomplete
tempted to address the concerns that vision or active limb          understanding to what extent the limb motion sense is al-
motion contributed to or was responsible for the kinaesthetic       tered by PD, but in a recent study, Konczak, Krawczewski,
impairments. These studies investigated kinaesthetic sensi-         Tuite, and Maschke (2007) investigated the sensitivity to
tivity of PD patients under conditions of blocked vision and        detect passive limb motion. They assessed blind-folded par-
those in which the patients were not actively moving and mus-       ticipants for their ability to detect motion of their arm placed
cle activation was monitored. Using a passive motion appara-        in a passive motion apparatus, which horizontally extended
tus, Maschke, Gomez, Tuite, and Konczak (2003) examined             or flexed the elbow joint at a range of velocities between
the sensitivity of PD patients to detect small changes in limb      1.65◦ /s and 0.075◦ /s. PD patients needed significantly larger
position by passively displacing the forearm at velocities less     limb displacements before they could judge the presence of
than 0.5◦ /s. After each displacement (between 0.2–8.0◦ ), par-     passive motion. With decreasing velocity, the detection time
ticipants indicated whether their forearm had been moved.           increased exponentially in both control and PD participants.
They tested three groups: individuals with mild to moderate         However, in comparison with healthy controls, the detec-
PD, patients with spinocerebellar ataxia, and control partici-      tion times of the PD group were increased 92–166% for the
pants. The detection thresholds at the 75% correct response         various velocity conditions.
level were 1.03◦ for controls, 1.15◦ for cerebellar patients,          A third aspect of kinaesthesia, the sense of heaviness, was
and 2.10◦ for PD patients, indicating that the PD group had         recently evaluated in mild to moderately affected PD patients
elevated detection thresholds that were on average twice as         (Maschke, Tuite, et al., 2006). The sense of heaviness is
high as the control and the cerebellar patient group. Only          related to the perception of weight. Maschke, Tuite, et al.
at displacements greater than 5◦ did PD patients exhibit the        determined psychophysical thresholds for detecting weight
same sensitivity as controls and cerebellar patients (see Fig-      sensations by applying a gradually increasing load to the
ure 2). This kinaesthetic impairment significantly correlated        index finger by means of two slings of different width (low vs.
with the severity and duration of PD (r = –0.7, for both mea-       high skin pressure). Although healthy age-matched control
sures). In a similar study, Putzki et al. (2006) replicated these   participants sensed a load at 31–33 g, the mean thresholds for
findings for the index finger, indicating that the sensitivity for    the PD group were significantly increased in both pressure
                                                                    conditions (48–52 g). The increase in detection thresholds
                                                                    correlated positively with the severity of PD as measured
                                                                    by the Unified Parkinson’s Disease Rating Scale, indicating
                                                                    that the sensitivity to detect a load decreases as the disease
                                                                    progresses.
                                                                       Further evidence for altered proprioceptive sensitivity in
                                                                    PD comes from a study investigating haptic acuity. Using a
                                                                    robotic manipulandum to create virtual contours, Konczak,
                                                                    Li, Tuite, and Poizner (2008) assessed the ability of PD and
                                                                    control participants to judge, without vision, the curvature
                                                                    of their arm passively or actively moved in a concave or
                                                                    convex trajectory. Of 11 PD patients, 9 (82%) showed ele-
                                                                    vated thresholds for detecting convex curvatures in at least
                                                                    one test condition. The respective median threshold for the
                                                                    PD group was increased by 343% when compared with the
                                                                    control group, indicating that the acuity of the haptic sense
                                                                    becomes reduced in PD. That the patients in the previously
   FIGURE 2. Forearm position sense acuity. The forearm
   was passively moved to 10 different positions (elbow joint       mentioned studies were only mildly to moderately affected
   angular displacement 0.2–8◦ ). Graph shows the sensitivity       underlines the notion that haptic as well as kinaesthetic im-
   functions of healthy control participants (N = 11), a group      pairments may become manifest already in the early stages
   of cerebellar patients (N = 9), and a group of mild to moder-    of the disease. That is, proprioceptive or kinaesthetic deficits
   ately affected Parkinson’s disease (PD) patients (N = 9). The    can appear very early in the disease and may precede motor
   perceptual detection threshold was defined at 75% correct
   response level. Each data point represents the mean response     deficits. However, current clinical examination protocols are
   rate of each group (reprinted with permission, M. Maschke,       not sensitive enough to detect these perceptual abnormalities.
   C. M. Gomez, P. J. Tuite, & J. Konczak, 2003).                      Because all of the previously mentioned psychophys-
                                                                    ical studies involved no active motion, monitored for

December 2009, Vol. 41, No. 6                                                                                                  545
J. Konczak et al.

unwanted muscle activity, and excluded vision, it is very           Jackson, Harrison, Henderson, & Kennard, 1995; Muratori,
unlikely that bradykinesia, tremor, or possible movement            McIsaac, Gordon, & Santello, 2008; Schettino et al., 2006),
compensation strategies can explain the reported decline in         for the coordination of arm and trunk motion (Poizner et
kinaesthetic sensitivity in PD. Moreover, these data argue          al., 2000), sequential arm movements (Curra et al., 1997),
that these kinaesthetic deficits are genuine manifestations          walking (Lewis, Byblow, & Walt, 2000), or for compensat-
of the disease that may occur very early in the disease             ing for mechanical perturbations (Jacobs & Horak, 2006). In
process and may even precede the known motor problems               reaching movements, for example, PD patients are impaired
in PD.                                                              when they cannot see their arm and thus must use proprio-
                                                                    ception to guide their reaches (Adamovich et al., 2001; see
                                                                    Figure 3).
  Sensorimotor Integration: The Link Between
                                                                       Likewise, when holding an object, afferent information
Vision, Proprioception, and Motor Function in PD
                                                                    from the digits must be mapped onto motor commands spec-
   Multiple lines of evidence indicate that the basal ganglia       ifying appropriate force levels. PD patients tend to develop
are important for sensorimotor integration, the mechanisms          elevated grip force levels when holding an object, despite
by which sensory information is processed to guide motor            the fact that they show both predictive and reactive modes of
planning and execution. Single cell recordings in the striatum      force control (Mueller & Abbs, 1990; Nowak & Hermsdor-
of rats, cats, and monkeys have demonstrated that the activ-        fer, 2006). Again, this suggests that their dysfunction consists
ity of these cells depends on whether sensory information           of defective central processing or gating of sensory input.
is linked to movement (Alexander & Crutcher, 1990; Lid-             PD patients also show deficits in visual saccades (Briand,
sky & Manetto, 1987; Lidsky, Manetto, & Schneider, 1985;            Hening, Poizner, & Sereno, 2001; Briand, Strallow, Hening,
Schneider et al., 1987; West et al., 1987). Striatal cells can be   Poizner, & Sereno, 1999; Chan, Armstrong, Pari, Riopelle,
silent for a given sensory event but robustly active when that      & Munoz, 2005; Hood et al., 2007; Shaunak et al., 1999).
same sensory event functions as a cue for a movement (West          Orienting to an environmental event with a saccade requires
et al., 1987). In addition, the caudate nucleus and substantia      integration of multimodal sensory information and a mech-
nigra contain a large proportion of cells that are multisen-        anism that controls the integration process to select a signal
sory, cells that could be used to integrate sensory inputs          (Hikosaka, Takikawa, & Kawagoe, 2000). Consistent with
and form a multimodal representation of the environment             a deficit in sensorimotor integration, PD patients’ voluntary
in the basal ganglia (Nagy, Eordegh, Paroczy, Markus, &             as opposed to reflex saccades are often markedly disrupted
Benedek, 2006). Likewise, the primate putamen contains bi-          (Briand et al., 2001, 1999).
modal visual-tactile cells that provide a map of peripersonal          Thus, PD may be considered, in part, as a disorder of
visual space. This map of visual space is organized somato-         gain control of sensorimotor integration (Kaji, 2001; Kaji,
topically and “could function to guide movements in the an-         Urushihara, Murase, Shimazu, & Goto, 2005). Within this
imal’s immediate vicinity” (Graziano & Gross, 1993, p. 96).         process, dopamine may help to set the threshold for this gain
When basal ganglia processes become disrupted, such as in           control by modulating the responsiveness of the organism to
MPTP-treated parkinsonian monkeys, more pallidal neurons            the environment (Schultz, 2007). Dopamine depletion in PD
than normal respond to passive limb movement, suggesting            then would disrupt the integration of environmental context
an impaired gain mechanism because of dopamine deple-               with action planning and execution.
tion (Filion et al., 1988). Results from other animal studies          Although the deficient sensory gating hypothesis points to
corroborate this finding by showing that the ability to use          a sensory origin of the motor symptoms, it fails to explain
posture-relevant sensory information decreases with striatal        why proprioceptive function seems to be especially affected
dopamine loss (Henderson, Watson, Halliday, Heinemann,              by PD. As outlined previously, numerous studies and clini-
& Gerlach, 2003; Martens, Whishaw, Miklyaeva, & Pellis,             cal observations confirm that PD patients may rely on visual
1996). Thus, there is a wealth of evidence that the basal gan-      cues to initiate or maintain movements. This visual depen-
glia receive suitable inputs from vision and proprioception         dence is consistent with a loss of proprioceptive function and
to play an important role in the sensorimotor integration and       points to a largely intact visual function in PD. Such vision-
that dopamine depletion negatively impacts this integration         for-proprioception compensation strategy indirectly implies
process.                                                            that a major basal ganglia function is proprioceptive-motor
   The pattern of deficits in PD is consistent with a disrup-        integration, whereas visuomotor integration is accomplished
tion of this integration mechanism. PD patients may become          elsewhere in the brain. There is some neuroanatomical ev-
increasingly dependent on external stimuli to initiate and          idence to support this claim. The basal ganglia receive af-
shape motor output and may be unable to effectively execute         ferents from the whole cortical mantle including the visual
movements when deprived of critical proprioceptive infor-           cortex, yet the projections from the dorsal visual stream to the
mation. This leads to a documented dependence on visual             basal ganglia are minor compared with the visual afferents
cues during reaching movements (Adamovich et al., 2001;             to the cerebellum (Glickstein, 2000). These cerebellar and
Flash, Inzelberg, Schechtman, & Korczyn, 1992; Klock-               posterior parietal circuits are known to be critical for on-line
gether & Dichgans, 1994), grasping movements (Jackson,              visuomotor control and may be largely spared by the disease,

546                                                                                                     Journal of Motor Behavior
                                                                       Proprioception and Motor Control in Parkinson’s Disease

                                                                    showed that, unlike healthy controls, PD patients do not
                                                                    modify postural response synergies immediately following a
                                                                    change in initial support conditions (Chong, Horak, & Wool-
                                                                    lacott, 2000; Chong, Jones, & Horak, 1999). For example,
                                                                    when healthy participants change postural support from free
                                                                    stance to sitting or to holding onto a stable support, their
                                                                    postural response synergies change immediately from leg to
                                                                    trunk or arm muscle activation (Horak, Nutt, & Nashner,
                                                                    1992). In contrast, participants with PD do not reduce leg
                                                                    postural responses in the first trial after a change in initial
                                                                    support condition of sitting or holding, although they grad-
                                                                    ually adapt postural synergies with practice (Chong et al.,
                                                                    1999; Horak et al.).
                                                                       Similarly, healthy participants, but not PD participants,
                                                                    scale up the size of their anticipatory postural adjustments
                                                                    prior to step initiation in the first trial following an increase
                                                                    in stance width (Rocchi et al., 2006). The immediate increase
                                                                    in lateral reactive force to unload the initial stance leg with
                                                                    a wide stance, compared with a narrow stance, requires pro-
                                                                    prioceptive mapping of initial body posture and modification
                                                                    of postural adjustments prior to any feedback from body mo-
                                                                    tion. In addition, the inability to quickly increase anticipatory
                                                                    postural adjustments when stance width increases also may
                                                                    be related to bradykinetic force output. However, regardless
                                                                    of the mechanism, such failure to make anticipatory postural
                                                                    adjustments to unload the stepping leg may be responsible
                                                                    for the compensatory narrow stance width, start hesitation,
   FIGURE 3. Participants reached in the dark to five remem-
                                                                    or freezing in advanced PD.
   bered or actual targets presented in three-dimensional space
   with a robot arm. The target was an illuminated LED. There          Two recent studies showed that PD patients have abnormal
   were three conditions of visual feedback in which partici-       postural coordination only when vision was obscured, which
   pants were provided either no vision during the movement,        is consistent with impaired proprioceptive mapping compen-
   only vision of the moving fingertip, or only vision of the        sated by use of vision of the body. In one study, healthy,
   target but not the arm. Arm trajectories and endpoints across
                                                                    age-matched participants could accurately direct their auto-
   trials and conditions are presented for a control participants
   (top panel) and a Parkinson’s disease (PD) participant (bot-     matically triggered, compensatory steps onto a small target
   tom panel). Green spheres represent movement endpoints           on the ground in response to external postural perturbations,
   when participants reached to remembered targets without          even when they could not view their stepping leg. In con-
   vision of their arms. Gray spheres represent movement end-       trast, PD patients consistently undershot the targets when
   points when participants reached to remembered targets with
                                                                    they could not see their legs (Jacobs & Horak, 2006). Sim-
   vision of their moving fingertips, and blue spheres represent
   movement endpoints when participants reached to a visually       ilarly, when PD patients closed their eyes, they showed a
   present target without vision of their arms. PD patients were    breakdown in the temporal coordination between postural
   impaired in the two conditions in which they could not see       adjustments and arm reaching during whole body reaching
   their arms. Thus, in reaching to remembered or to actual         to a target (Tagliabue, Ferrigno, & Horak, 2009).
   targets, PD patients have difficulty in extracting and using
                                                                       Postural kinaesthesia also is disrupted in patients with PD.
   critical information from proprioception to map arm posi-
   tions onto spatial target locations to guide reaching move-      Horak and coworkers tested the ability of PD patients to per-
   ments (adapted from S. V. Adamovich, M. B. Berkinblit, W.        ceive surface inclination by asking blindfolded, standing par-
   Hening, J. Sage, & H. Poizner, 2001).                            ticipants to compare the relative dorsiflexion or plantarflexion
                                                                    of the support surface under a test foot with a 4-degree tilt of
                                                                    the surface under the reference foot (Wright et al., 2006). Par-
which could explain the increased reliance on vision by PD          ticipants with PD showed fewer percent correct trials when
patients.                                                           indicating whether the surface under the reference foot was
                                                                    more or less plantar-flexed or dorsiflexed than the surface un-
                                                                    der the test foot (see Figure 4). Impaired kinaesthesia of the
Proprioceptive Deficits and Postural Control in PD
                                                                    support surface was significantly correlated with the severity
  Several deficits of postural coordination observed in PD           of PD. It is noteworthy that levodopa medication did not im-
patients are consistent with the hypothesis that they have          prove this kinaesthestic deficit, although it generally led to
an impaired proprioceptive body map. A series of studies            better motor performance.

December 2009, Vol. 41, No. 6                                                                                                   547
J. Konczak et al.

                                                                    like the postural deficits associated with peripheral, propri-
                                                                    oceptive deficits that cause prolonged postural response la-
                                                                    tencies that are not observed in PD (Cameron, Horak, &
                                                                    Herndon, 2009; Inglis, Horak, Shupert, & Jones-Rycewicz,
                                                                    1994).



                                                                        Effects of Levodopa and DBS on Motor and
                                                                                  Proprioceptive Function
                                                                       Dopamine replacement therapy is highly effective in ame-
                                                                    liorating many symptoms in PD. It is especially effective
                                                                    in early PD and results in an improvement of quality in
                                                                    life and survival (Miyasaki, Martin, Suchowersky, Weiner,
                                                                    & Lang, 2002). However, the effects of levodopa on pro-
   FIGURE 4. Kinaesthesia impairment during stance in par-
                                                                    prioception are not fully understood. Jobst, Melnick, Byl,
   ticipants with Parkinson’s disease in the on- and off-
   levodopa state compared with age-matched controls for per-       Dowling, and Aminoff (1997) concluded that levodopa does
   ception of surface inclination (A) and torso rotation (B). (A)   not improve kinaesthetic deficits in PD. During their on-
   Percent correct in judging one more degree of surface dor-       medication state and with vision occluded, PD patients did
   siflexion in test compared with reference foot. (B) Percent       not improve their sensitivity to perceive differences in move-
   correct in judging left or right direction of torso rotation.
                                                                    ment amplitudes made to a target away from the body, a task
                                                                    requiring the reliance on proprioceptive feedback (Jobst et
                                                                    al.). There is some indication that levodopa actually may
   The same group tested the kinaesthesia of axial trunk ro-        have an added detrimental effect on kinaesthesia in PD.
tation by asking participants to indicate the direction and         For example, when comparing PD patients between their
initial detection of yaw oscillations (1◦ /s) of the support sur-   off- and on-medication states, arm proprioception was im-
face under their feet during stance (Wright et al., 2006). Axial    paired by 31% 1 hour after administration of levodopa or
rotation occurred either at the trunk, by stabilizing the shoul-    dopamine agonists (O’Suilleabhain et al., 2001). In contrast,
ders to earth and the pelvis to the rotating surface, or hips,      psychophysical studies found no significant correlations be-
by stabilizing the pelvis to earth (Gurfinkel et al., 2006). The     tween levodopa dosage and elevated detection thresholds for
ability of PD patients to accurately detect the direction and       arm position sense, arm motion sense, or weight perception
onset of axial rotation was impaired for both trunk and hip         in a group of medicated and de novo (i.e., nonmedicated) PD
twisting (see Figure 4), indicating that trunk position sense       patients (Maschke et al., 2003; Maschke, Tuite, et al., 2006).
was compromised. This finding corroborates and extends the              In summary, there is some evidence that levodopa fur-
results of previous studies showing that upper limb position        ther degrades proprioceptive acuity with some authors ar-
sense is altered by PD (Maschke et al., 2003; Maschke, Tuite,       guing that levodopa enhanced proprioceptive deficits might
et al., 2005).                                                      be one key in the development of levodopa induced dysk-
   When vision is absent, the control of sway on a firm sur-         inesia (O’Suilleabhain et al., 2001). A role of levodopa in
face depends primarily on proprioceptive feedback, whereas          phasic pharmacological reduction of proprioception would
control of sway on an unstable surface depends on vestibular        be further supported if nondopaminergic medication such as
feedback. The fact that PD patients may show larger postural        amantadine was shown to improve proprioception. However,
sway compared with controls when standing on a firm surface          the only study investigating the influence of nondopaminer-
than when standing on an unstable surface with eyes closed          gic medication on proprioception revealed no influence of
also is consistent with poor use of proprioceptive feedback         the NMDA-antagonist flupirtine on automatic postural re-
but excellent use of vestibular information, to control postu-      sponses in PD (Putzki, Maschke, Drepper, Diener, & Tim-
ral sway. In fact, sway characteristics of patients with PD are     mann, 2002).
consistent with increased proprioceptive feedback loop noise           Although levodopa is a very effective treatment for PD,
with abnormal feedback gain (Maurer, Mergner, & Peterka,            motor complications develop over time with its use. The
2004).                                                              complications include the development of fluctuations in re-
   Thus, proprioceptive deficits may affect postural stability       sponse to medication (i.e., motor fluctuations) and the ap-
in PD by impairing (a) adaptation to changing support con-          pearance of medication-induced abnormal involuntary move-
ditions, (b) accuracy of compensatory stepping, (c) coupling        ments (i.e., dyskinesia). In addition, antiparkinsonian medi-
between postural adjustments and voluntary movement, (d)            cation is not always that effective in treating tremor. Thus, as
the perception of trunk and surface orientation, and (e) pos-       the disease progresses, a subset of patients with PD become
tural sway in stance. These postural deficits suggest a deficit       candidates for DBS neurosurgical treatment, which can be
in central integration of proprioception because they are un-       very effective in alleviating motor certain symptoms in PD

548                                                                                                     Journal of Motor Behavior
                                                                       Proprioception and Motor Control in Parkinson’s Disease

(Samii, Nutt, & Ransom, 2004). Since the first documented           the related tactile and haptic senses progressively diminishes
report on the effects of DBS of the subthalamic nucleus (STN       in PD (Konczak et al., 2007, 2008; Maschke et al., 2003;
DBS) for PD (Limousin et al., 1995), there have been many                                                                  a
                                                                   Maschke, Tuite, et al., 2006; Maschke et al., 2005; Pr¨ torius
reports on the efficacy of STN DBS for improving limb move-         et al., 2003; Putzki et al., 2006). If, as suggested, a main
ment in patients with PD. For example, STN DBS has been            pathomechanism of PD lies in altering the gain of gating
shown to be efficacious for simple force generation across          and integrating proprioceptive and other sensory informa-
a variety of effectors (Alberts, Elder, Okun, & Vitek, 2004;       tion (Abbruzzese & Berardelli, 2003; Kaji et al., 2005), it
Brown et al., 1999; Pinto, Gentil, Fraix, Benabid, & Pollak,       becomes plausible that a failure to evaluate and map pro-
2003; Wenzelburger et al., 2003). It also has been shown           prioceptive information onto voluntary and reflexive motor
to be effective for single joint ballistic movements involv-       commands underlies many of the observed motor symptoms
ing either the elbow or ankle joint (Vaillancourt et al., 2006;    in PD. Levodopa medication may further decrease propri-
Vaillancourt, Prodoehl, Verhagen Metman, Bakay, & Corcos,          oceptive sensitivity, which would then explain the decrease
2004). These studies of single joint movement have shown           in postural stability commonly observed in levodopa med-
that STN DBS causes dramatic changes in both the agonist           icated PD patients (Beuter, Hernandez, Rigal, Modolo, &
and antagonist muscle activation that underlie the changes         Blanchet, 2008; Horak, Frank, & Nutt, 1996; O’Suilleabhain
in motor performance. STN DBS also has been shown to be            et al., 2001). In contrast, STN DBS improves propriocep-
efficacious for much more complicated movements such as             tive acuity, which may explain the reported positive effect on
movements performed in a sequence to a series of targets           some aspects of postural function (Guehl et al., 2006; Rocchi,
(Agostino et al., 2008).                                           Chiari, Cappello, Gross, & Horak, 2004). However, the im-
   Although numerous studies have shown that DBS may               proved kinaesthetic function because of STN DBS does not
improve motor symptoms in PD, especially tremor, little is         translate necessarily into improved postural function. Thus,
known about the direct effect of DBS on proprioception. A          the effects of other interventions such as STN DBS on pro-
recent psychophysical experiment determining limb position         prioceptive sensitivity and posture require further evaluation.
detection thresholds in more severely affected, medicated
PD patients reported a 20% improvement in kinaesthetic                               ACKNOWLEDGMENTS
acuity during DBS on-state when compared with DBS-off
(Maschke, Tuite, Pickett, Wachter, & Konczak, 2005). How-            The idea for this review originated from an international
ever, during DBS, forearm position sense acuity was not fully      workshop on Motor Control and Proprioception in Parkin-
restored and the mean threshold of the PD patient group was        son’s Disease, which was held in Minneapolis on September
still twice as high as the threshold of healthy control group.     18–19, 2008. All authors attended this workshop that was
Given that levodopa potentially decreases kinaesthetic acuity      supported in part by the Minnesota Medical Foundation, the
in some PD patients (O’Suilleabhain et al., 2001), the pos-        University of Minnesota Center for Clinical Movement Sci-
itive effects of DBS on kinaesthetic acuity may have been          ence, the University of Minnesota Academic Health Center,
further enhanced, if the patients also were tested in their off-   and by the University of Minnesota School of Kinesiology.
medication state. However, the lack of clinical improvements       Aspects of the research were supported in part by NIH grants
in kinesthesia after DBS surgery is consistent with the lack of    NS036449 (HP) and NS40902 (DMC).
improvement in postural control and speech and the increase
in falls with DBS.
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552                                                                                                             Journal of Motor Behavior

				
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