Reader Benefit: People with Parkinson disease make hypometric perceptual distance misjudgments that can interfere with their performance on activities of daily living as well as instrumental activities, and may have dangerous consequences.
ANOVA=analysis of variance; PD=Parkinson disease; SD=standard deviation.
Correctly guiding the body in the environment requires the ability to make appropriate size estimates of both body parts and distances in surrounding space. Studies showing discrepancies between body size and spatial estimates suggest that these capacities may be impaired in people with Parkinson disease (PD) (Lee et al, 2001). PD is also associated with hypometric movements, movements that fall short of the goal. Such movements improve with external cueing, suggesting that a cognitive impairment may be contributing to the movement hypometria (Morris et al, 1996; Oliveira et al, 1997). Skidmore et al (2009) demonstrated that patients with PD have a conceptual hypometria. Our major aim in this study was to learn whether the neural representations of body size and position (body schema) are also hypometric in patients with PD and, if so, how this egocentric (arm’s length) hypometria compares to estimates of allocentric (extrapersonal) standard units of distance.
Desmurget et al (2003, 2004) suggested that the hypometric movements associated with PD may result from impairments in the basal ganglia’s ability to modulate planned movements appropriately, particularly when patients cannot see where they are moving. Although some studies suggest that these impairments result from motor dysfunction (Desmurget et al, 2003, 2004) as well as deficits in sensorimotor integration (Contreras-Vidal and Gold, 2004; Moore, 1987), the mechanisms underlying these behavioral phenomena are not fully understood. Also unknown is the degree to which these decrements result from motor system impairments, perceptual-attentional impairments, or impairments at the representational level, including body schema.
Body schema is a dynamic representation that allows for continuous adjustments of body parts and posture, based on multimodal afferent inputs that inform the mental representations of changes in the relative relationships of body parts to each other and to the external environment (Contreras-Vidal and Gold, 2004; Coslett et al, 2002; Frederiks, 1969; Gallagher, 2005; Goldenberg, 2005; van Beers et al, 2002). There are several reasons to suspect that patients with PD have impairments in body schema, including alterations of proprioception (Contreras-Vidal and Gold, 2004; Zia et al, 2000), visuospatial perception (Harris et al, 2003), and integration of kinesthetic signals (Contreras-Vidal and Gold, 2004). Perturbations of body schema representations may also influence motor planning and actions (Boecker et al, 1999; Contreras-Vidal and Gold, 2004).
Many patients with PD have an asymmetry of signs and symptoms between their left and right sides at the onset of their disease, and later asymmetry of severity; thus, it is possible that these asymmetries contribute to impairments in body-spatial computations. The right hemisphere appears to be dominant in mediating spatial cognition (De Renzi, 1982). Lee et al (2001) found that patients who had more pronounced PD signs on the left than the right side of their body overestimated the size of a doorway opening relative to their body, and those with more pronounced right-sided signs underestimated the size of the doorway relative to their body. Lee’s study, however, did not resolve the question of whether the impairments reflected misjudgment of body size or of the size of the external objects such as the doorway opening.
Klockgether and Dichgans (1994) showed that after patients with PD saw a target and then reached for it without being able to see it (open looped movement), they undershot the mark, suggesting that either they misperceived their limb length (thinking it longer than it really was) or they misperceived the space (underestimating the distance to be traveled).
Harris et al (2003) noted that patients with more pronounced PD signs on their left side showed significant impairments in visual perception such that “objects appeared smaller in the left and upper visual spaces….” Shenker et al (2004) showed that healthy participants were more accurate at estimating distance in peripersonal space using an arm’s length than using standard units of 1, 2, and 3 feet; the investigators suggested that their results supported the postulate that the brain has 2 distinct representations of space. These findings have been replicated in a larger study by some of the same authors (Kesayan et al, 2010).
The purpose of our current study was to test the hypothesis that when patients with PD estimate distance, they are less accurate when using a body-centered method of measurement, such as arm’s length, than when using standard units of distance. We used the methods outlined by Kesayan et al (2010) and Shenker et al (2004) to compare 3 participant groups: patients with PD whose signs were worse on the left side, patients with PD whose signs were worse on the right side, and healthy controls. We tested all the participants’ abilities to estimate distance on both the left and right sides of their body using estimates of their right and left arm’s length as well as standard units of distance.
We recruited the participants, all native English speakers, from the North Florida/South Georgia Veterans Affairs Medical Center. The patients had been diagnosed with idiopathic PD using the Brain Bank criteria (Hughes et al, 1992).
We screened all potential participants for gross cognitive impairment with the Mini-Mental State Examination (Folstein et al, 1975), and excluded those with a score <27. We also gave all potential participants the Geriatric Depression Scale, long form (Yesavage et al, 1983), and excluded those with a score in the abnormal range. Other exclusion criteria were a history of substance abuse, stroke, psychosis, head trauma, or learning disability, and taking medications that could influence cognition.
After excluding candidates who had evidence of depression or did not complete the study, we had 20 patients with PD. We assessed these patients with the Unified Parkinson’s Disease Rating Scale while they were on their dopaminergic medications; 12 had more severe PD signs on the right side of their body and 8 had more severe PD signs on their left side.
Of 18 people who volunteered to serve as control participants, we excluded 5 because of depression. We matched the 13 remaining controls by age and education level to the patients with PD. Table 1 shows the participants’ sex distribution and the mean and standard deviations (SD) of their age, years of education, Mini-Mental State Exam scores, Geriatric Depression Scale scores, Unified Parkinson’s Disease Rating Scale scores, Hoehn and Yahr Scale, and years since the diagnosis of PD.
This study was approved by the University of Florida Institutional Review Board. All participants signed informed consent forms.
We tested the participants in a room with plain white walls. We covered the floor with brown butcher paper so the tiles would not be visible. Before starting testing, we explained all procedures. Then, to eliminate visual cues, we fitted the participants with a neck collar wide enough to block their view of the floor.
As shown in Figure 1, we positioned the participants with the lateral portion of their right or left shoulder (or arm) either beside the wall or 5 feet away from the wall, and with their midsagittal plane parallel to the wall. We asked them to turn their head 90 degrees toward the wall, so that their face and eyes were parallel to the wall. We asked them to keep their arms adducted at the shoulder with all the other upper extremity joints being fully extended, so that their arms were always “by their sides.”
In the egocentric condition, testing the participants’ estimates of their arm length, we asked them to move so that the distance between the outside of their shoulder and the wall would be the length of their arm when it was abducted at their shoulder with the other joints fully extended, ie, the entire upper limb was perpendicular to the wall and the side of their body. In the allocentric condition, testing the participants’ estimates of standard units of distance, we asked them to move either toward or away from the wall so that the outside of their shoulder closest to the wall would be 1, 2, or 3 feet from the wall. The participants had to do both tasks by estimating the distances, without moving their arms.
Each participant completed a total of 48 experimental trials, with 12 trials for each of 4 starting positions: right shoulder beside the wall, left shoulder beside the wall, right shoulder 5 feet from the wall, and left shoulder 5 feet from the wall. From each of these 4 starting positions, the participants were asked to position themselves such that they were 1, 2, or 3 feet or an arm’s length from the wall. Each of these test conditions was repeated 3 times in each starting condition. We randomized the order of all trials.
After each trial, when the participants had repositioned themselves, we used a measuring tape to find the distance between the outside of their shoulder and the wall. During this measurement, the experimenter stood behind the participants, so as not to give them any feedback about the accuracy of their position. After all 48 trials were completed, the experimenter determined the “correct” arm’s length by measuring the distance between the outside of the participant’s shoulder and the wall when the arm was fully extended and abducted so that the fingertips were just touching the wall.
We converted all distances to millimeters before comparing the measurements using analysis of variance (ANOVA).
We considered results significant at P<0.05.
To evaluate our hypothesis that PD affects egocentric (arm’s length) and allocentric (standard units of distance) computations differently, we compared the accuracies of the patients and controls in these 2 experimental conditions. To control for the influence of longer distances (eg, 3 feet vs 1 foot) on error magnitudes, we calculated absolute average error ratios for both measures:
Thus, those error ratios that are closer to 0 represent more accurate performance.
We compared the mean arm’s length error ratio and the mean standard units of distance ratio using ANOVA. The patients with PD were significantly less accurate than the controls in estimating their arm’s length (patients’ mean arm’s length ratio=0.1223, SD=0.08; controls’ mean arm’s length ratio=0.0669, SD=0.05; F1,32=5.381, P=0.027). The patients were also less accurate at estimating standard units of distance (patients’ mean standard units of distance ratio=0.2186, SD=0.05; controls’ mean standard units of distance ratio=0.1591, SD=0.04; F1,32=12.947, P=0.001).
To learn whether the patients made significant hypometric or hypermetric distance estimation errors in the egocentric and allocentric conditions, we compared the patients to the controls on the direction of error. Again, we calculated error ratios, but we accounted for direction to control for the influence of different distances on error magnitudes, ie, we did not determine absolute values, but rather:
The patients were more hypometric (mean arm’s length ratio=−0.0900, SD=0.10; standard units of distance error ratio=−0.1287, SD=0.11) than controls (mean arm’s length ratio=−0.0056, SD=0.08; standard units of distance error ratio=−0.0531, SD=0.11) in their distance estimations in both the egocentric and allocentric conditions (F1,31=20.227, P<0.001). Both groups were more hypometric in standard unit than arm’s length estimations (F1,31=5.599, P=0.024). There was, however, no significant difference in the relative magnitude of hypometria between the standard units and arm’s length distance estimates as a function of group.
To evaluate whether the patients with worse PD signs on their left side performed differently on their arm’s length and standard units of distance estimations from the patients with worse PD signs on their right side, we compared these subgroups on absolute errors in both the arm’s length and standard units conditions, directional errors in both conditions, and both absolute and directional errors with left- and right-sided estimates. We also compared the patients’ laterality effects with the controls’.
We did not find any significant laterality effects between the patients with more severe left-side versus right-side parkinsonian signs. For arm’s length estimates, when compared to the controls, the patients were less accurate (absolute values) at right-sided than left-sided distance estimates (F1,33=3.145, P=0.043) (patients’ mean right arm’s length error ratio=0.1134, SD=0.083; patients’ mean left arm’s length error ratio=0.0017, SD=0.06; controls’ mean right arm’s length error ratio=0.0679, SD=0.048; controls’ mean left arm’s length error ratio=0.0165, SD=0.057).
We did not find any significant right-left differences for standard units of distance (patients’ mean right standard units error ratio=0.2242, SD=0.061; patients’ mean left standard units error ratio=0.1680, SD=0.041; controls’ mean right standard units error ratio=0.1503, SD=0.043; controls’ mean left standard units error ratio=0.1367, SD=0.04).
To learn whether there was a relationship between the relative lateral severity of PD (independent of the right or left laterality of these signs) and estimates of arm’s length and standard units distances, we correlated the arm’s length and standard units ratios for the more-impaired side versus the less-impaired side. None of these correlations reached statistical significance.
For the analyses of the standard unit of distance estimations described up to this point, we combined the participants’ estimates of 1, 2, and 3 feet. To learn the influence of standard units magnitude, we analyzed separately the differences in estimates between patients and controls at 1 foot, 2 feet, and 3 feet (mixed design, repeated measures ANOVA). Both the patients and controls were increasingly hypometric in their estimates as the distance increased; however, the patients had a steeper slope of change (distance by group interaction) (F1.33,41.24=3.4, P=0.030).
Post hoc analyses, comparing performance between the groups at 1, 2, and 3 feet, showed that the patients were significantly more hypometric than the controls in their distance estimations at 3 feet, but the groups did not differ significantly at 1 or 2 feet (patients’ mean error ratio at 1 foot=0.0764, SD=0.155; controls=0.1073, SD=0.142, F1,31=0.332, P=0.568; patients’ mean error ratio at 2 feet=−0.1849, SD=0.122; controls=−0.1059, SD=0.115, F1,31=3.437, P=0.073; patients’ mean error ratio at 3 feet=−0.2872, SD=0.081; controls=−0.1706, SD=0.103, F1,31=13.205, P=0.001).
Finally, because we found hypometric differences in distance estimations between patients and controls as well as a progression of hypometria from 1 foot to 3 feet, we wanted to evaluate whether the observed hypometria was a result of attentional-conceptual or action-intentional demands. To that end, we compared the patients and controls on trials in which they had to estimate a distance of 1 foot from the wall. In 1 of these 1-foot estimates, participants standing with their shoulder beside the wall were asked to move their body so that their shoulder would be 1 foot away from the wall. In the other of these 1-foot estimates, participants standing 5 feet from the wall were asked to move 4 feet closer to the wall so that they would be 1 foot away from the wall. Our ANOVA revealed no significant difference as a function of magnitude of movement on these tasks, suggesting that the patients’ hypometric estimates were unlikely to be fully explained by a movement hypometria (ie, patients moving 1 foot error ratio=0.1583, SD=0.157; patients moving 4 feet error ratio=−0.0011, SD=0.185; controls moving 1 foot error ratio=0.1814, SD=0.142; controls moving 4 feet error ratio=0.0536, SD=0.129).
This study compared patients with PD and healthy controls in their abilities to estimate distances in their immediate surrounding external space, using 2 different frames of reference, arm’s length and the standard units of distance of 1, 2, and 3 feet. We posited that by asking participants to make spatial estimates using arm length as a reference, they would be forced to attend to and selectively activate a portion of their neural representation of their arm’s length in space (ie, their body schema). In contrast, we anticipated that when asked to estimate spatial distances using standard units of distance measured in feet, they would be forced to attend selectively to their neural representations of standard units of distance. From a neurologic perspective, these spaces correspond to personal and peripersonal space (Rizzolatti et al, 1997a; Sakata and Kusunoki, 1992), which are represented by discrete modular networks. We further speculated that the activated system of measurement would create a reference frame that would directly affect how participants computed the measured space between their shoulder and the wall.
Our patients with PD made more hypometric errors than our controls when estimating the space between their shoulder and the wall using either arm’s length or a standard unit of distance as their frame of reference. Like the controls, the patients were more accurate when making arm’s length estimates than when making estimates based on the standard units of feet. While the controls’ estimates of arm’s length and standard units differed significantly, the patients’ did not. Further, the patients were less accurate than the controls when estimating standard units of distance in right-side space, but not significantly less accurate on the left side. The severity of left- versus right-sided asymmetry of PD signs did not appear to be related to the laterality of errors in the patients’ estimates of arm’s length or standard unit distance.
In moving to their estimated position of their arm’s length or 1, 2, or 3 feet away from the wall, the patients often ended up too close to the wall. Even when they started 5 feet from the wall, they still moved too close to the wall. Therefore, their hypometria could not have been related to movement (motor hypometria), but must have been related to disorders of either attention or spatial representation. This finding is consistent with that of Skidmore et al (2009), who demonstrated that patients with PD have a conceptual hypometria. Demirci et al (1997) reported that patients with PD estimated distance normally when they depended on their vision, but when they made kinesthetic estimates they perceived the distances as shorter. We did not test kinesthesia, but we did find that our patients’ visual estimates of distance were hypometric.
We do not know why our patients with PD positioned themselves too close to the wall. There are several possibilities. Crucian et al (2000) suggested that visuospatial difficulties in PD are linked to executive dysfunction associated with disruption of frontal-basal ganglionic networks. Patients with frontal-subcortical dysfunction often demonstrate abnormal approach behaviors, such as grasp and utilization behaviors. Thus, it is possible that our patients with PD had a perceptual grasp behavior with the wall.
Another possible explanation is that our patients misperceived the distances. Distance misperceptions have several possible causes. Studies in which patients with neglect perform tasks such as line bisection have revealed that a hemispheric injury, which reduces the ability to attend to portions of a stimulus, reduces the perception of magnitude (Heilman et al, 2012). Thus, our patients’ spatial errors could theoretically be related to an increase in their attention to peripersonal space, a hypothesis that will need to be further tested.
Skidmore et al (2009) found that, even in the absence of environmental stimuli, patients with PD made hypometric estimates when asked how far they needed to extend their arms to perform certain tasks (eg, eating, hanging clothes on a line to dry). Because those patients were not required to use visual information to guide their estimates, the results cannot be explained by a hypothetical disorder of visual perception or attention. In both the Skidmore et al study and our study, the participants had to rely on their spatial representations of their arm’s length and of standard units of distance. It is, therefore, possible that patients with PD have inattention to or an impaired ability to activate and assess the magnitude of these spatial representations.
The body schema is a complex representation stored in cortical-subcortical neural networks (Holmes and Spence, 2004; Làdavas and Serino, 2008). Input to these networks includes both sensory and motor information, reflecting the current state of the body and limbs in anticipation of future movements (Làdavas and Serino, 2008; Rizzolatti et al, 1997b). Much of the literature about the neural representations of space surrounding the body (peripersonal space) also suggests that the brain considers this space from a self- or body-oriented perspective (Colby and Duhamel, 1996; Rizzolatti et al, 1997b). The neural representations of peripersonal space help to program neuronal firing in response to the perceived proximity of an object and with respect to a specific body part (Colby and Duhamel, 1996; Farnè et al, 2005; Làdavas and Serino, 2008; for review, Rizzolatti et al, 1997b; Sakata and Kusunoki, 1992).
Polymodal cells integrate information from the visual, tactile, and auditory sensory modalities, to provide information about a given event in the context of multiple discrete body-part-specific spatial reference frames. Each frame is organized to reflect the way information is considered with respect to a specific body part, such as the limbs, head, eyes, or trunk (Fogassi et al, 1996). The information from these discrete frames of reference is then translated and integrated into a common reference frame (Buneo and Andersen, 2006).
The posterior parietal cortex is a major polymodal association area, and studies of neural representations of body schema and space have focused on the role of the posterior parietal cortex (Avillac et al, 2004; Bremmer et al, 2001; Cardinali et al, 2009; Colby, 1998; Colby and Duhamel, 1996; Corradi-Dell’Acqua et al, 2009; Farnè et al, 2005; Felician et al, 2004; Holmes and Spence, 2004; Làdavas and Serino, 2008; Pellijeff et al, 2006; Rizzolatti et al, 1997a, 1997b; Sakata and Kusunoki, 1992; Save and Poucet, 2009) and the frontoparietal circuits (Rizzolatti et al, 1997b, Làdavas and Serino, 2008, for review) in storing and processing these representations. This network, which contains integrated multimodal sensory information, provides a unified, context-specific representation of space that can inform motor planning networks, thus controlling the execution of body and limb movements in that space (Rizzolatti et al, 1997a). In this way, body schema, spatial representations, motor planning, and execution are functionally linked.
In summary, patients with PD who were on their dopaminergic medications made hypometric spatial errors when estimating distances, whether estimating their arm’s length or standard units of distance as their frame of reference. Against our expectations, we found no relationship between the relative lateral severity of PD and the estimates of egocentric and allocentric distances. Our failure to find a more modular disorder might have resulted from the overall under-representation of patients with more severe PD signs. Overall, however, our findings are consistent with the observation of Skidmore et al (2009) that hypometria in PD is not directly related to the motor deficits of PD but may be related to disordered perception, attention, or spatial representations.
Our results may have important pragmatic implications. For example, because patients with PD must routinely interact with environmental stimuli, an inability to estimate distances correctly can have important and even dangerous consequences. The neuronal mechanisms accounting for hypometria in PD remain unclear, and further research is needed to elucidate the pathophysiology of this hypometric perceptual disorder.
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