Exp Brain Res (2012) 223:259–269 DOI 10.1007/s00221-012-3256-8
RESEARCH ARTICLE
The influence of spatial working memory on ipsilateral remembered proprioceptive matching in adults with cerebral palsy Daniel J. Goble • Micah B. Aaron • Seth Warschausky Jacqueline N. Kaufman • Edward A. Hurvitz
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Received: 26 July 2012 / Accepted: 31 August 2012 / Published online: 14 September 2012 Ó Springer-Verlag 2012
Abstract Somatosensation is frequently impaired in individuals with Cerebral Palsy (CP). This includes the sense of proprioception, which is an important contributor to activities of daily living. One means of determining proprioceptive deficits in CP has been use of an Ipsilateral Remembered (IR) position matching test. The IR test requires participants to replicate, without vision, memorized joint/limb positions previously experienced by the same (i.e. ipsilateral) effector. Given the memory component inherent to this task, the present study sought to determine the extent to which IR proprioceptive matching might be influenced by known spatial working memory deficits. Eleven adults with CP underwent IR elbow position matching, where blindfolded individuals were given either a short (2 s) or long (15 s) duration to memorize the target elbow angle. A standard clinical measure of spatial working memory (i.e. Corsi block-tapping task) was also administered. The results showed that the directional (i.e. constant) error produced across trials did not differ between the short and long target duration conditions. However, it was found that participants were significantly more consistent in their matches (i.e. had
D. J. Goble (&) Sensory-Motor and Rehabilitative Technology Laboratory (SMaRTlab), School of Exercise and Nutritional Sciences, College of Health and Human Services, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182-7251, USA e-mail:
[email protected] M. B. Aaron School of Kinesiology, University of Michigan, Ann Arbor, MI, USA S. Warschausky J. N. Kaufman E. A. Hurvitz Department of Physical Medicine and Rehabilitation, University of Michigan, Ann Arbor, MI, USA
smaller variable errors) when given more time to encode proprioceptive targets in the long duration condition. The benefit of having more time was greatest for those individuals with the highest variable errors in the short target condition, and a significant association was seen between improvements in variable error and greater performance on 4/5 spatial working memory measures. These findings provide the best evidence to date that IR position matching tests are influenced by spatial working memory. Keywords Proprioception Spatial working memory Cerebral palsy Sensory assessment Kinesthesia Joint position sense
Introduction The incidence of Cerebral Palsy (CP) is approximately 1 in every 300 live births, and that number appears to be rising (Odding et al. 2006; Yeargin-Allsopp et al. 2008). CP has traditionally been associated with motor impairments that are attributed to brain injury during the first few years of life (Keogh and Badawi 2006). Beyond motor deficits, individuals with CP also commonly exhibit reduced cognitive function and sensory abilities, regardless of the extent and location of brain injury (Odding et al. 2006). This is likely due to global, neurophysiological changes that happen throughout the brain in CP, including loss of gray matter (i.e. neurons), fewer glial cells and a reduction in neuronal connections (Inder et al. 1999; Folkerth 2005; Nagae et al. 2007; Kurz and Wilson 2011). In the 1950s, the first reports surfaced indicating a high prevalence of somatosensory deficits in CP (Tizard and Crothers 1952; Hohman et al. 1958; Tachdjian and Minear 1958). These studies suggested that as many as 70 % of
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individuals with CP had some form of deficit in their ability to perceive somatosensory signals arising from stimulation of the skin, muscle and/or joint receptors. One specific deficit that was highlighted in this work was the sense of proprioception, or the ability to perceive joint/limb positions and movement in the absence of visual feedback. Proprioception is thought to play a vital role in movement production, acquisition and the refinement of motor skill (Rothwell et al. 1982; Sainburg et al. 1995; Vercher et al. 2003). As such, proprioceptive deficits have significant implications for individuals with CP, including the performance of many activities of daily living (KrumlindeSundholm and Eliasson 2002; Arnould et al. 2007). To date, the assessment of proprioceptive ability in CP has relied heavily on ‘‘movement detection’’ tests (e.g. Tizard and Crothers 1952; Tachdjian and Minear 1958; Kenney 1963; Twitchell 1966; Van Heest et al. 1993; Cooper et al. 1995; Klingels et al. 2010). In these tests, participants are asked to close their eyes and indicate over several trials whether an imposed movement of a given body part (typically the finger) has occurred. The direction of the movement (e.g. flexion/extension) is also usually indicated. While this test is an effective means of determining whether the proprioceptive pathway is intact, it is not a particularly good indicator of proprioceptive acuity per se. Rather than providing a sensitive measure of the degree of proprioceptive ability across individuals, this test gives only binary information regarding whether proprioception is present or not. An alternative to movement detection proprioceptive tests is the joint/limb ‘‘position matching’’ test (e.g. Opila-Lehman et al. 1985; Wann 1991; van Roon et al. 2005; Chrysagis et al. 2007; Goble et al. 2009a; Wingert et al. 2009; Smorenburg et al. 2011, 2012). This test, which has gained increasing popularity in the past several decades, consists of providing a reference joint angle or limb position to the test participant and then asking them to replicate it in the absence of vision. The reference can be specified in several ways, using either visual feedback or proprioception or both. Regardless, the measured difference between the reference and matching limb positions provides a graded measure of error, which can be used to represent the degree of proprioceptive acuity within and across individuals. Despite providing a potentially better means of proprioceptive acuity assessment, position matching tests are not without limitations. Of particular relevance to previous studies of proprioceptive function in CP is the use of ‘‘ipsilateral remembered (IR)’’ matching paradigms. In this type of matching test, the researcher typically brings the participant to a target joint/limb position and allows them to experience it without vision for several seconds. The joint/limb is then moved away from the target location by the researcher and, after a short delay, the participant must replicate without vision the reference position with the
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same (ipsilateral) joint/limb based on spatial working memory. Given the inherent spatial working memory demands of the IR test, a recent perspective paper emphasized that IR matching tests should be utilized with caution, particularly in populations of individuals prone to memory dysfunction (Goble 2010). In this case, it is likely that the results of IR proprioceptive tests do not reflect proprioceptive acuity alone but, also, the inability to encode, retain and recall spatial location information in spatial working memory. Evidence supporting the idea that IR matching tests of proprioception are inherently influenced by spatial working memory was recently provided in healthy young adults (Goble et al. 2010). In this study, the amount of time participants who had to memorize unseen target elbow angles in an IR position matching test was either a more typical 3 s or a much longer 12 s duration. The results showed that giving participants more time at the target significantly reduced the variable errors made when matching memorized, target joint angles. It was therefore concluded that greater time at the target during IR matching allowed individuals to develop a more complete representation of joint position in spatial working memory. This result implies that a more accurate assessment of proprioceptive ability might be obtained in IR matching tests when longer target durations are utilized. One limitation of the Goble et al. (2010) study was that healthy adults were tested, who likely exhibited only small differences in working memory ability. In this case, it was not possible to fully determine the relationship between varying levels of spatial working memory ability and IR matching errors. In the present study, we aimed to resolve this limitation by correlating, for the first time, IR matching performance with a measure of spatial working memory ability (i.e. Corsi block-tapping test) in a group of adults with CP, who are known to vary on both factors. We hypothesized that not only smaller IR errors would be seen when participants were given more time to develop a memory-based representation of proprioceptive targets, but also, importantly, improvement in matching performance with increased target duration would be associated with spatial working memory ability. Taken together, these results would provide the strongest evidence to date regarding the potential role spatial working memory plays in the performance of IR proprioceptive tests.
Methods Participants Informed consent was obtained from 11 adults (6 males; 5 females) with CP between the ages of 18–50 years
Exp Brain Res (2012) 223:259–269 Table 1 Participant sensorimotor status information
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Participant
Diagnosis
Modified ashworth score
MACS
GMFCS
Dominant arm
AROM (flexion/ extension)
1
Hemiplegia
1
II
I
Left
152/0
2
Diplegia
0
I
II
Left
140/0
3
Diplegia
0
II
III
Left
140/0
4
Diplegia
0
II
II
Right
140/0
5
Diplegia
0
I
I
Right
140/0
6
Diplegia
0
II
IV
Right
143/0
7
Diplegia
1
I
I
Left
140/-20
8
Hemiplegia
0
II
II
Right
140/0
9
Hemiplegia
0
II
I
Right
144/-12
10
Diplegia
0
II
I
Right
140/0
11
Diplegia
0
II
III
Right
140/-10
(mean ± SD age = 33.0 ± 10.3 years) to participate in the study. Eligibility for the study included a diagnosis of CP by a medical professional in the University of Michigan Health System and the ability to complete all experimental tasks. Persons were excluded if they had a history of upper limb surgery, major trauma, or botulinum toxin injections within the 6 months prior to testing. Detailed information regarding each participant’s sensorimotor status is provided in Table 1 including (1) diagnosis (hemiplegia vs. diplegia), (2) modified Ashworth score for spasticity (Bohannon and Smith 1987), (3) manual ability classification system score (Eliasson et al. 2006), (4) gross motor function classification (Palisano et al. 1997), (5) dominant arm as determined by the Edinburgh Handedness Inventory (Oldfield 1971) and (6) active elbow range of motion for the dominant arm. All procedures were approved by the University of Michigan Institutional Review Board. Procedure IR proprioceptive matching test The apparatus for the proprioceptive matching test has been described previously in detail (Goble et al. 2005, 2009b; Goble and Brown 2007, 2008). In short, participants were seated with their dominant forearm resting on an adjustable horizontal aluminum lever that pivoted about the elbow joint over a near frictionless ball bearing. The dominant (i.e. less affected) arm was selected for use over the non-dominant (i.e. affected) arm, as it was thought that this limb would provide the most conservative estimate of proprioceptive deficits and would be less likely to be confounded by motor impairments. The starting posture was such that the shoulder was rotated 15° in the horizontal plane (i.e. horizontal adduction) and placed in approximately 80° of abduction. The elbow was extended 100°, and participants were neutral at the wrist. During testing, a
potentiometer below the pivot point of the elbow was used to record elbow angle in real time to a laptop computer with precision of 0.1°. In order to eliminate visual feedback during the IR test, participants were blindfolded while seated at the experimental apparatus. IR matching trials were performed in the following fashion. First, the experimenter moved the lever under the participant’s forearm via a handle until the elbow joint was at a reference angle of 20 or 40° more extended than the starting position. This target was held for either 2 s (i.e. short target duration) or 15 s (i.e. long target duration) while the participant encoded the location in working memory based on proprioceptive information from the limb. The forearm was then moved back to its starting position by the experimenter and, after a 2 s delay, the participant was verbally asked to ‘‘Match’’ the memorized elbow angle through his or her own forearm movement. The participant was given unlimited time to reach a stabilized matching position, at which point the forearm was rotated back to the starting elbow angle by the experimenter. The two target duration conditions (i.e. short vs. long) in this experiment were presented in a blocked fashion with target magnitude (i.e. 20 vs. 40°) randomized and balanced within each condition. Half of the participants performed matching of the short target duration trials first, and half the participants performed the short target duration trials last. Eight trials were performed in each target duration condition, and there was no evidence of learning over the course of the experiment, presumably due to a lack of feedback given to the participant regarding matching performance (i.e. no knowledge of results). The number of trials per target duration condition (i.e. n = 8) was based on previous studies showing that stable measures of proprioceptive error can be obtained with five or more matching trials (for review see Goble 2010). The chosen number of trials also ensured that the testing session was kept short enough to maximize participant attention throughout.
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For all trials, participants were given the option to repeat the trial if they felt it did not represent their best performance. However, only one repeated trial occurred over the course of the entire experiment (i.e. less than 0.5 % of trials). Participants were also given a number of practice trials (n = 8) to ensure that they understood the task and to allow them to become familiar with the experimental equipment. Practice trials were conducted within the same range, but not necessarily equal to the experimental target angles (i.e. 20–40°). No feedback on practice performance accuracy was given. To increase participant understanding during practice, trials were performed without a blindfold, thus allowing full visual feedback to be available throughout the reference and matching portions of the matching trial. Spatial working memory test Following the IR proprioceptive matching test, participants were given 5–10 min of rest before undertaking a widely used clinical test of spatial working memory. This assessment, the Corsi block-tapping task (Corsi 1972; Kessels et al. 2000), was conducted in accordance with the methods described by Wechsler (1981). Briefly, participants were seated across the table from the experimenter with a 28 9 21 cm rectangular board with ten 3 9 3 9 3 cm numbered cubes attached to it placed between them. The number side of the blocks faced the experimenter, and the blocks were placed in pseudo-random locations across the board. The goal of the Corsi block-tapping test was to determine the largest sequence of blocks the participant could encode, maintain and recall in spatial working memory. To accomplish this, participants watched on successive trials as the experimenter tapped on a predetermined sequence of blocks at a rate of one per second. On each trial, participants with CP were asked to reproduce with the dominant arm either the same exact sequence (i.e. Forward Spatial Span) or the reverse sequence (i.e. Backward Spatial Span) based on spatial working memory. Forward spatial span was always tested first, and backward spatial span, last. Both forward and backward span testing began with sequences of two blocks, which were increased by one block when participants were successful on at least one of two attempts at that sequence length. Participants were informed when an additional block would be added to the sequence. When two failed attempts occurred at a particular sequence length, the test was terminated. Data analysis Elbow angle data from the proprioceptive matching trials were filtered with a second-order low-pass Butterworth filter (zero phase lag, cutoff frequency = 12) and post-
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processed using customized routines developed in LabVIEW (National Instruments, Texas). Reference and matching elbow angles were determined from the derivative of the position signal (i.e. velocity), using an algorithm that determined the last data point prior to the arm being moved back to the starting arm posture. Specifically, the velocity signal had to differ by at least 2 standard deviations from the mean velocity value of the arm calculated at rest in the first 200 ms of the trial (e.g. Goble and Brown 2008; 2009; Goble et al. 2010). Two matching error measures were calculated to indicate proprioceptive accuracy. First, constant error was calculated as the difference between the final matching elbow angle and the target elbow angle in degrees. This signed measure of error allowed for directional accuracy to be determined, such that positive error values indicated target overshooting (i.e. the elbow extended too far) and negative values target undershooting (i.e. the elbow did not extend far enough). The second proprioceptive measure calculated was variable error in degrees. This measure was determined as the standard deviation of the constant error across trials within a target duration condition. Variable error is an accepted measure of target matching consistency (i.e. variability) from trial to trial. For the spatial working memory test (i.e. Corsi blocktapping test), five measures of performance were determined as defined by Wechsler (1981). The first two were the longest forward and backward spatial spans, respectively, calculated as the maximum number of blocks in a forward or backward sequence that a participant could remember. The second two measures were the spatial span forward and backward total raw scores, which were determined by adding up the total number of correct trials on the forward and backward aspects of the test, respectively. Lastly, a total raw score for the spatial span test was taken as the sum of the total number of correct trails on both forward and backward aspects of the test. Statistics IR proprioceptive matching performance measures (i.e. constant and variable errors) were submitted to separate one-way analyses of variance (ANOVA) with repeated measures for the factor target duration (i.e. 2 vs. 15 s). A two-tailed alpha for this test was set at p \ 0.05. For the variable error measure, there was an obvious effect of target duration, and thus, difference scores were subsequently calculated for this measure by subtracting variable error in the 2 s condition from the 15 s condition. These difference scores provided a single measure indicating the amount of improvement that was demonstrated by each participant when given more time to encode the target elbow angle in the long target duration condition.
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The variable error difference score (i.e. variable error improvement) was utilized for two types of correlational analyses. First, variable error improvement was correlated with variable errors in the 2 s target duration condition. This statistical test sought to determine whether a significant relationship existed between the amount of improvement in variable error with greater target duration and the amount of initial error in the shorter (i.e. 2 s) duration condition. Second, improvement in variable error with increased target duration was correlated with the 5 measures of spatial working memory derived from the Corsi block-tapping test. This analysis was conducted to determine whether spatial working memory could explain a significant proportion of the IR proprioceptive matching performance. All correlations were considered significant with respect to a two-tailed alpha of p \ 0.05.
Results Longer target duration times reduce IR variable errors The mean (± standard error) constant and variable error values for the short (i.e. 2 s) and long (i.e. 15 s) target duration conditions are shown in Figs. 1 and 2, respectively. In the case of constant error, no significant effect of target duration was found for directional matching accuracy (F1,10 = 3.0, p = 0.11). Specifically, individuals with CP produced similar constant errors on the short and long target duration conditions which, on average, were not significantly different than zero. These near zero values indicate that there
Fig. 1 Mean ± standard error (between subjects) of the constant errors seen for IR proprioceptive acuity in the two (i.e. short vs. long) target duration conditions
Fig. 2 Mean ± standard error (between subjects) of the variable errors seen for IR proprioceptive acuity in the two (i.e. short vs. long) target duration conditions
was no population bias in terms of undershooting versus overshooting the target position, regardless of the amount of time given to memorize the target. In contrast to constant errors, variable errors were significantly influenced by the amount of time participants had to encode the target position (F1,10 = 15.5, p \ 0.01). When given a longer (i.e. 15 s) target duration, individuals with CP had variable errors that were 44 % smaller than when a shorter (i.e. 2 s) duration was given at the target. As shown in Fig. 3, there was also a significant relationship between the amount of individual improvement in variable error when more time was given at the target (i.e. 15 – 2 s
Fig. 3 The relationship between variable error on the short duration target (i.e. 2 s condition) and improvement in variable error when more time was allowed (i.e. 15 s condition – 2 s condition)
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performance) and the amount of variable error in the short duration condition (r = 0.93, p \ 0.001). This relationship was such that those individuals with the highest errors in the 2 s condition benefited the most from having increased time at the target to encode elbow position. Fig. 4 The association between improvement in variable error with greater time at the target (i.e. 15 s condition – 2 s condition) and the 5 measures of spatial working memory derived from the Corsi block-tapping task. Asterisk healthy population mean from Monaco et al. (in press); Double asterisk healthy population mean from Wilde et al. (2004)
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Spatial working memory ability predicts longer target duration improvement As shown on the y-axis of the graphs in Fig. 4, participants with CP demonstrated a range of performances on the test
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of spatial working memory (i.e. Corsi block-tapping test). This spread allowed for subsequent correlations to be made between the amount of individual improvement in variable error with longer target durations (i.e. 15 – 2 s performance) and performance on the Corsi block-tapping test. As a point of comparison, population means from two large samples of healthy adults (Wilde et al. 2004; Monaco et al. in press) are shown in Fig. 4 to demonstrate the relative impairments of the various participants with CP in this study. In the forward spatial span task, more than half (6/11) the participants fell below the population mean value for the longest sequence (population mean = 6.0) and the raw score (population mean = 8.0) metrics. In the backward spatial span task, all but one (10/11) participant was below the population mean for longest sequence (population mean = 5.2) and raw score (population mean = 6.7) metrics. All but one (10/11) participant was below the population mean (14.7) for the total span raw score as well. Of the five spatial working memory measures calculated (i.e. longest forward spatial span, longest backward spatial span, forward span raw score, backward span raw score and total raw score), four were found to have a significant relationship with the amount of improvement in variable error seen when more time at the target was given (Fig. 4). Only the longest forward digit span (Fig. 4a) did not explain a significant amount of variance related to improvement on the task with more target time—although a similar trend to other variables was seen. The greatest correlation was found for the total raw score measure (Fig. 4e; r = -0.78, p \ 0.05). This was followed by the backward span raw score (Fig. 4d; r = -0.74, p \ 0.05), longest backward spatial span (Fig. 4b; r = -0.67, p \ 0.05), forward span raw score (Fig. 4c; r = -0.53, p \ 0.05) and longest forward spatial span (Fig. 4a; r = -0.48, p = 0.08), respectively.
Discussion Somatosensory impairment is highly prevalent in individuals with CP (e.g. Tizard and Crothers 1952; Hohman et al. 1958; Tachdjian and Minear 1958; Jones 1976; Tardieu et al. 1984; Yekutiel et al. 1994; Cooper et al. 1995; Wingert et al. 2009). This includes the sense of body position and movement (i.e. proprioception), which is known to play an important role in the performance of activities of daily living that require acquisition and refinement of motor skill (Rothwell et al. 1982; Sainburg et al. 1995; Krumlinde-Sundholm and Eliasson 2002; Vercher et al. 2003; Arnould et al. 2007). In the present study, spatial working memory ability was shown to influence proprioceptive acuity when measured using an IR matching test. Specifically, it was found that participants
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with CP had smaller variable errors when afforded more time to memorize target elbow angles. Further, there was a relationship between the amount of improvement in variable error with longer target durations and spatial working memory performance on several aspects of the Corsi blocktapping task. These results build on those previously reported for healthy adults (Goble et al. 2010) and strongly suggest that IR proprioceptive matching tests are influenced by spatial working memory. Opila-Lehman et al. (1985) provided the first known report of IR proprioceptive matching ability in individuals with CP. In this study, a kinesthesiometer was used to measure the accuracy of internal and external rotations about the shoulder in a sample of 12 children with spastic CP, 12 children with athetoid CP and 12 age-matched typically developing children. The results showed clear differences in IR matching ability, as evidenced by significantly greater errors in both spastic and athetoid groups of individuals with CP. In this case, the authors noted that ‘‘the kinesthetic (IR) task used in this study required kinesthetic perception as well as recall of limb position’’. Further, they felt that it was still ‘‘necessary to determine whether poor performance on this (IR) task is due to inaccurate perception, lack of sensory-motor memory, inability to access this memory or interaction of all these’’. The present results support and extend this line of thinking, showing that IR matching ability is improved with greater time to develop a representation of the target position, and an association between spatial working memory and improvement on the IR test with greater target duration. A more recent study involving the IR position matching abilities of individuals with CP was performed by Goble et al. (2009a). In this study, a small sample of children with hemiplegia was tested on an IR elbow angle matching study similar to that in the present study. In this case, however, only a 2 s target duration was provided, and a comparison was made between the matching abilities of individuals with primarily right versus left hemisphere injuries. The results of this study suggested that a hemispheric difference existed in matching performance such that right, but not left, brain damage was associated with proprioceptive deficits. To this extent, it is interesting to note that there is the literature showing that the right hemisphere has an important role in spatial working memory recall tasks including those that involve kinesthesia and position sense (Leonard and Milner 1991a, b, 1995). It might therefore be proposed that the hemispheric asymmetries suggested by Goble et al. (2009a) were not solely due to proprioceptive issues, but rather, a reflection of greater damage to parts of the brain devoted to spatial working memory. Indeed, Smorenburg et al. (2011, 2012) recently found no evidence of a difference in proprioceptive acuity related to side of brain injury when a
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non-memory-based matching test of proprioception was utilized in a group of children with CP. The present study represents the first known assessment of proprioceptive matching ability in adults with CP. This population of individuals was selected: first, because of known deficits in spatial working memory (e.g. Gagliardi et al. 2011), and second, because they are under-represented in all aspects of the CP literature. There is little reason to believe that the pattern of results shown in the present work would differ for other, more typically studied populations of individuals with CP (i.e. children and adolescents). Rather, the influence of age would likely only shift the magnitude of the effects seen, such that the present findings for mature adults might be conservative in nature compared to individuals with CP still undergoing development. A comparison can be made between the effect of target duration time in the present study and that reported for healthy young adults by Goble et al. (2010). This study found a similar, although less pronounced, improvement in variable errors with longer (12 s) target durations as compared to shorter (3 s) target durations. The magnitude of variable errors in the longer target duration condition of the present study (mean = 2.6°) are very similar to those found in the Goble et al.’s (2010) study (mean across targets = *2.5°), suggesting a normalization of performance with increased target duration time. Indeed, it is only when participants were given a shorter amount of time to memorize the target that these studies appear to demonstrate a difference between healthy adults and those with CP (healthy mean across targets = *3.2°; CP mean = 4.6°). While a clear relationship has been shown between spatial working memory and variable errors on an IR position matching task, a question remains as to what is the actual mechanism underlying this finding. Tardieu et al. (1984) showed that the fidelity of proprioceptive signals is reduced in children with CP when a muscle tendon vibration technique was used to stimulate muscle spindle receptors and induce movement illusions in the upper limb. If proprioceptive signals are, indeed, ‘‘noisier’’ in CP, it would stand to reason that even a healthy brain might require more time to develop a clear representation of the joint angle to be matched. Alternatively, it may be that the peripheral, proprioceptive signals in individuals with CP remain intact, but additional time at the target is needed to compensate for a deficient spatial working memory system to encode the joint angle information. One limitation of the present study was that the extent and location of brain injury was relatively unknown in the population of individuals with CP tested. Despite this, a consistent pattern of results was obtained for the various experimental manipulations studied, which may actually make the present findings more robust. Emerging
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neuroimaging work using vibration to stimulate proprioceptors in the upper and lower extremities has shown that processing of position-related proprioceptive information occurs in multiple brain areas (Naito et al. 2005, 2007; Goble et al. 2011, 2012a). This includes traditional somatosensory areas such as Brodmann area 3a, the secondary somatosensory cortex and the supplemental motor area. In addition, a right lateralized attention network has been identified that includes regions of the dorsolateral prefrontal cortex, insula and the putamen of the basal ganglia. Given the extent of this network, it is likely that most, if not all, individuals with CP have at least some damage to tissue typically devoted to proprioceptive function. Future work aimed at connecting brain structure, neural activity and behavioral measures of proprioceptive acuity is no doubt necessary to disambiguate the central origin of proprioceptive deficits in CP. Beyond constant and variable error measures of IR proprioceptive matching, it is not uncommon for absolute (unsigned) error to be reported. Absolute error represents a complex combination of variable and constant errors, and when constant errors approach zero, absolute error will reflect variable error (Shultz and Roy 1973). This was the case in the present study, and thus, no absolute errors were reported, as this information was deemed redundant. Further, known differences in proprioceptive error exist based on the passive/active nature of the reference and target matching movements, with active matching of an active reference producing the least error. Given the repeated measure design of this experiment, however, the specifics of the matching paradigm would not likely change the main findings regarding the relationship between spatial working memory and IR proprioceptive matching error. Rather, alternative methods of generating the target and reference position would only serve to influence the overall magnitude of the errors produced and not the pattern of results. The Corsi block-tapping test utilized in this study consisted of a motor component that may have influenced results. However, any motor deficits that existed were likely mitigated by having participants perform the task with the dominant (i.e. less affected) arm. Indeed, this strategy has been used successfully by several researchers in the past (e.g. Gagliardi et al. 2011; Kessels et al. 2000), and no overt problems in reaching were observed in the present study. In addition, the accuracy demands for completing the Corsi block-tapping movements were low, given the overall spacing of the blocks themselves and their relative size. Participants were also unconstrained by any speed or reaction time requirement and could thus correct any unlikely mistake do to motor deficits that may have occurred. A similar argument can be made for the IR matching task response movements, where participants moved at a self-selected pace and were afforded unlimited
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time to correct the limb position, should they have perceived making a motoric error. Future work is required to determine whether the present results might be applicable to other memory-based tests of somatosensory function, such as force matching (Rameckers et al. 2005; Smits-Engelsman et al. 2005) or tactile sensitivity (Sanger and Kukke 2007). However, given similar findings linking spatial working memory and arithmetic accuracy in the cognitive domain (Jenks et al. 2007, 2009), it would appear that the present findings may be far reaching and part of a global mechanism of functional impairment. To this extent, recent basic science studies employing memory-based tests of proprioception in healthy young adults (e.g. Jones and Henriques 2010; Wilson et al. 2010; Jones et al. 2012) and more clinical work addressing, for example, proprioceptive function in the elderly (e.g. Adamo et al. 2007, 2009; Goble et al. 2012b), and Parkinson’s disease (e.g. Poizner et al. 1998; Adamovich et al. 2001) may benefit from a similar investigation into the influences of spatial working memory on proprioceptive ability. This is particularly true with respect to the latter populations, as both have been shown to demonstrate varying degrees of memory impairment (see for reviews Iachini et al. 2009; Dubois and Pillon 1997).
Conclusion Proprioceptive assessment in individuals with CP that uses an IR matching test approach should be viewed with caution, given the present findings regarding the influence of spatial working memory. In the case where this test is performed with a relatively short hold time (*2–3 s), it is likely that the consistency (i.e. variable error) of matching performance will be reduced due to limits in spatial working memory, rather than any reduction in the proprioception. In this case, proprioceptive assessments using an IR matching paradigm with a short duration are prone to overestimating deficits in proprioception in individuals with CP and, possibly, other clinical populations. It is recommended that longer duration targets be utilized by clinicians and researchers to minimize the influence of spatial working memory on IR tests. Acknowledgments Special thanks to Susan Brown for use of the Motor Control Laboratory in the School of Kinesiology at the University of Michigan. This work was supported, in part, by a fellowship award to D. Goble by the Canadian Institutes for Health Research— Institutes for Aging.
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