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Article Excerpt
The basal ganglia circuit plays a fundamental role in the preparation of a response. Individuals with Parkinson's disease (PD) are considered to have difficulty with two particular aspects of response preparation, namely, the maintenance of cognitive and motor sets and the ability to adequately switch between cognitive and motor sets. The vast majority of substantiating evidence derives from limb motor control, electrophysiological, and neuropsychological research. These investigations have begun to unfold the characteristics and mechanisms of aberrant response processing in PD. The putative deficits of response preparation are likely tied to the impaired processing of internally versus externally generated cues and are discussed in this larger context. Despite the relevance of response "maintenance" and "switching" to the preparatory aspects of speech, little research has been conducted in this area. However, extant investigations on the preparatory aspects of cognitive and motor responses in PD can provide a theoretical basis for rehabilitation strategies. Clinical implications and management suggestions are highlighted.
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Idiopathic Parkinson's disease (PD) is traditionally viewed as a disorder of motor control that affects the execution of movement. However, there are strong arguments for additional disruption during response preparation. Overarching themes from neuroimaging, movement disorder, and neuropsychological research suggest that prior to movement, individuals with PD have reduced ability to maintain a prepared response or to switch from a prepared response to a novel response. These deficits arise from both motor and cognitive processes. To date, the potential influence of these preparatory deficits on the communicative function of people with PD has been largely ignored, despite the relevance of "maintenance" and "switching" impairments to the preparatory aspects of speech. Many questions remain unanswered regarding the presence or nature of these deficits as they pertain to verbal communication.
The purpose of this article is to summarize the empirical basis for the reported abnormalities of response maintenance and switching in PD. A review of musculoskeletal and neuropsychological studies is presented along with supportive evidence from related fields. This summary is followed by a discussion of the well established difficulty of individuals with PD to perform internally generated versus externally guided behaviors and how this difficulty relates to maintenance and switching anomalies. Finally, recommendations for rehabilitation are offered based on the theoretical and clinical support for these deficits of response preparation.
RESPONSE MAINTENANCE
One of the primary functions of the basal ganglia is to maintain prepared movements prior to action (Morris & Iansek, 1996). Support for this critical role has derived from diverse areas of investigation, including single cell recordings of neural activity in nonhuman primates (Alexander & Crutcher, 1990; Jaeger, Gilman, & Aldridge, 1993; Schulz & Romo, 1992), cerebral blood flow analysis (Deiber, Ibanez, Sadato, & Hallet, 1996; Horwitz, Deiber, Ibanez, Sadato, & Hallet, 2000; Jueptner & Weiller, 1998), functional neuroimaging (Menon, Anagnoson, Glover, & Pfefferbaum, 2000; Postle & D'Esposito, 1999), and human motor performance (Agostino, Berardelli, Formica, Accornero, & Manfredi, 1992). Further evidence stems from investigations of response maintenance in individuals with PD. Keeping a prepared response in an appropriate state of readiness involves the maintenance of motor and cognitive preparations (Stern, Horvitz, Cote, & Mangels, 2005), and both have been shown to be problematic for individuals with PD.
Maintenance of a Motor Set
Studies of limb control have identified deficits of response maintenance in PD. Preparing a response requires the activation and maintenance of the appropriate action schema or motor program (Berardelli, Rothwell, Thompson, & Hallet, 2001; Stuss, Shallice, Alexander, & Picton, 1995). To assess this process, the primary methodologies employed have been kinematic analyses of arm movements, reaction time analyses of button/handle press tasks, and electrophysiological studies. Across investigations, the implementation of a delay period before the response has often helped to identify the loss of motor preparation.
Kinematic studies have utilized execution tasks that allow inferences regarding the motor preparation process. Romero, Van Gemmert, Adler, Bekkering, and Stelmach (2003) studied the effect of prolonging the time a hand remains immobilized on an aiming movement performed by participants with PD and elderly controls. The authors concluded that the delay period affected the ability of participants with PD to plan the movement. Specifically, individuals with PD exhibited a decay in position sense over a 6- and 10-second delay period, as measured by variables such as the length of the primary submovement. Importantly, when the delay was minimal (1 sec), participants with PD and the controls performed similarly. Two kinematic investigations also were conducted by Gentilucci and Negrotti (1999a, 1999b). Participants with PD were able to plan a sequential action as suggested by the change in the initial kinematics of the movement based on the extrinsic properties of the first and second targets. According to the authors, however, the motor program decayed during its execution and only properties of the first target were taken into account. In contrast, the kinematics of control participants remained affected by the properties of both the first and second targets during the entire course of the reach. The authors speculated that individuals with PD have a deficit in storing and maintaining the plan of an action.
Reaction time (RT) methodologies also have been used in the examination of response maintenance. The consensus from many RT studies is that individuals with PD have difficulty maintaining the motor command at an appropriate state of readiness (Berardelli et al., 2001; Jones, Phillips, Iansek, & Bradshaw, 1992; Marsden, 1989). This finding is based on experiments that systematically manipulated interstimulus intervals (e.g., between a cue or prime and the target response), and/or compared performance on simple versus choice reaction time tasks (Bherer, Belleville, & Gilbert, 2003; Bloxham, Dick, & Moore, 1987; Jahanshahi, Brown, & Marsden, 1992, 1993; Sheridan, Flowers, & Hurrell, 1987).
The disruption to motor preparation also has been documented through electrophysiological studies using the Bereitschaftspotential (BP) and Contingent Negative Variation (CNV), which can be used to measure the cortical consequences of basal ganglia deficits. The BP is negative cortical electroencephalographic activity that precedes voluntary movement by approximately 1200-1500 msec, and systematically increases in amplitude up to the onset of movement (Brunia & van Boxtel, 2001). The early component of the BP is thought to reflect activity in the supplementary motor area (SMA), while the late component is thought to represent activity in the motor cortex (Marsden, 1989). The early component is defective in PD, with findings of lower BP amplitudes (Dirnberger, Reumann, Endl, Lindinger, Lang, & Rothwell, 2000; Haslinger, Erhard, Kampfe, Boecker et al., 2001). As the SMA receives considerable input from the basal ganglia, the results support the notion that the problem for individuals with PD is not as much with the very act of moving but with the processes leading to the movement (Day & Dick, 1990; Verleger, 2004). The CNV is a slow wave potential that occurs between a warning stimulus and an imperative stimulus in a reaction time task and is thought to reflect response preparation (Stern et al., 2005). The overall finding from studies that measured CNV before the imperative stimulus was a reduction in the amplitudes of participants with PD (Gerschlager, Alesch, Cunnington, Deecke et al., 2004). Thus, cortical activations during response preparation appear to be reduced in individuals with PD.
Parkinson's disease has thus been shown to affect the maintenance of motor preparation prior to a response, as well as during response execution. Explanations for this difficulty primarily entail a decay of activation of the motor program (Agostino et al., 1992; Berardelli et al., 2001; Gentilucci & Negrotti, 1999a, 1999b; Robertson & Flowers, 1990; Sheridan et al., 1987). Abnormally rapid motor program degradation in PD may be caused by increased system noise and interference due to programming of other responses (Sheridan et al., 1987). By extension, motor preparation may be affected by a decay of position sense (Romero et al., 2003). It is firmly established that individuals with PD have decreased proprioception (Jobst, Melmick, Byl, Dowling, & Aminoff, 1997; Schubert, Prokop, Brocke, & Berger, 2005) as well as deficits in the central processing and integration of kinesthetic information, which can abnormally alter the input to a motor plan (Contreras-Vidal & Gold, 2004).
Maintenance of a Cognitive Set
Executive function deficits are commonly documented in individuals with PD and may affect numerous processes including goal setting, initiation, inhibition, and planning behaviors. Cognitive set shifting and maintenance are included among these executive-type deficits and are particularly germane to the discussion of response preparation given their corresponding motor counterparts. Specific to maintenance of a cognitive set, individuals with PD have repeatedly evidenced difficulty with this process (Alevriadou, Katsarou, Bostantjopoulou, Kiosseoglou, & Mentenopoulos, 1999; Dubois & Pillon, 1997; Mollion, Ventre-Dominey, Dominey, & Broussolle, 2003, but see Lewis, Cools, Robbins, Dove, Barker, & Owen, 2003), as demonstrated by measures such as the Wisconsin Card Sorting Test (WCST; Heaton, Chelune, Talley, Kay, & Curtiss, 1993) and verbal fluency tasks (e.g., Ruff, Light, Parker, & Levin, 1996). Cognitive set may be defined as a state of brain activity that predisposes a person to respond in one way when several alternatives are available (Flowers & Robertson, 1985). Control of set involves maintaining one predisposition or "strategy" against other competing possibilities (that is, the equivalent of attention) (Flowers & Robertson, 1985). It has been suggested that individuals with PD are able to acquire mental sets, but have difficulty maintaining newly acquired sets against competing alternatives or in high interference conditions, suggesting a deficit in the internal control of attention (Dubois & Pillon, 1997;...
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