Visual inspection time in Parkinson’s disease: deficits in early stages of cognitive processing
Introduction
Inspection time (IT) is a simple information processing paradigm dependent on a participant’s ability to identify physical properties of a stimulus presented within a limited time interval (Deary & Stough, 1996, Nettelbeck, 1982, Vernon, 1986). In contrast with reaction time (RT) studies, the dependent variable of interest in an IT task is not related to the time required to select a motor response, nor the time required to transmit the selected motor response to the appropriate body segment. Measures of IT can thus be considered an important indicator of information processing speed, particularly with regards to the early, or input, stages (Petrill, Luo, Thompson, & Detterman, 2001).
The dissociation between information processing and speed of motor output is particularly interesting within populations demonstrating clinically impaired movement, such as Parkinson’s disease (PD). It is well documented that individuals with PD experience significant impairment on tests of simple RT (Gauntlett-Gilbert & Brown, 1998), and yet it is unclear whether such deficits can be interpreted as ‘pure’ slowness at the input stage, or a delay in the output of a selected motor response to the limb (Adams, Victor, & Ropper, 1997). To the extent, therefore, that IT is a valid predictor of information processing speed, it may be useful in distinguishing between bradykinesia (slowness of movement) and bradyphrenia (slowness of cognition) in PD.
Given its reliance on the speed at which participants can accurately apprehend the properties of a visually presented stimulus, IT is often described as a measure of perceptual speed. Although few previous studies have explicitly examined IT in PD, individuals with PD have been shown to have significant perceptual processing deficits. For example, Giaschi, Lang, and Regan (1997) tested a single individual with PD on a task requiring the identification of motion-defined letters and found that the patient required a longer stimulus presentation than age-matched controls. Interestingly, Giaschi et al. (1997) report that the introduction of dopaminergic medication did not improve the perceptual ability of the PD patient. While suggestive of an overall perceptual processing deficit in PD, it may also be indicative of poor occulomotor control, as the task required substantial stimulus tracking. Bachmann et al. (1998), however, demonstrated that individuals with PD are significantly slower on elementary visual recognition tasks, even when occulomotor motor demands of the task (i.e. stimulus tracking) are controlled. Furthermore, although medication was not directly manipulated, unmedicated (de novo) and medicated patients demonstrated similar perceptual processing deficits, supporting the basic findings of Giaschi et al. (1997).
Two recent studies have directly examined IT in individuals with PD. In the first study of this kind, Phillips et al. (1999) compared the visual IT of 16 individuals with PD to the performance of two sets of control participants: one group that was age-matched (n=16), and one group that was substantially younger (n=16). The PD patients were on their regular dopaminergic medications, and were considered to be “ON” at the time of testing. Participants were presented with two unlit LEDs, and were asked to judge the order of onset time between the LEDs as they were lit. Although elderly participants required significantly longer IT than the younger participants, no significant difference was observed between participants with PD and elderly participants. In a second study, Shipley, Deary, Tan, Christie, and Starr (2002) used Deary’s visual IT loop task (Deary, 1995) in comparing medicated individuals with PD, with healthy control participants. Participants were required to visually attend to four letters presented serially on a computer screen, and then recall the letter sequence after having seen the same sequence repeated four times. The inter-letter presentation time was manipulated systematically during the sequence presentations, and participants with PD required significantly longer presentation times than healthy control participants in order to successfully complete the task. More recently, Sawamoto, Honda, Hanakawa, Fukuyama, and Shibasaki (2002) employed a mental operations task to compare a PD group to a group of healthy control participants. Participants were required to serially update a mental representation in response to a visually presented command. Although this task requires significantly more cognitive processing than the traditional IT paradigm, it is noteworthy since individuals with PD demonstrated a significant impairment that worsened (relative to healthy participants) as the presentation duration was shortened. Although two out of these three studies suggest that IT deficits may be associated with PD, it is important to note that the only two studies demonstrating significant impairment for PD patients used a paradigm involving a substantial amount of higher-order cognitive processing, particularly short-term memory. Given that there is some evidence to suggest a short-term memory deficit in PD (e.g. Cooper & Sagar, 1993), it remains to be demonstrated that PD patients have an IT deficit that is distinct from memory impairment.
IT has been proposed to be a good chronometric indicator of the integrity of the cholinergic system (Nathan & Stough, 2001), and deficits in IT have been demonstrated in patients with Alzheimer’s disease (Deary et al., 1991, Schlotterer et al., 1984), as well as in healthy participants following the administration of a nicotinic acetylcholine antagonist (Thompson, Stough, Ames, Ritchie, & Nathan, 2000). It has also been demonstrated that the deficits produced by acetylcholine antagonism in healthy participants are partially reversed through the administration of cholinergic agonists (Stough et al., 1995, Thompson et al., 2000; Thompson, Wilby, & Stough, 2002). Given that there is a loss of nicotinic acetylcholine receptors (nAChRs) in nigrostriatal pathways in PD (Court et al., 2000, Perry et al., 1995; Rinne, Myllykyla, Lonnberg, & Marjamaki, 1991), one might also expect IT deficits in PD. Further to this, one would expect that these deficits to be relatively intractable to treatment with levodopa, as IT performance has been proposed to be independent of dopamine levels in healthy participants (Stough et al., 2001, Stough et al., 2001). The purpose of this study, therefore, is to investigate the extent to which IT is impaired in PD, as well as the extent to which IT is affected by the administration of levodopa.
Section snippets
General method
Two studies were conducted during the course of the present research. In the first study, healthy control participants and individuals with PD were evaluated on the inspection time task in an ‘optimally medicated’ state (i.e. participants were experiencing a qualitative “ON” period). In the second study, participants with PD were evaluated with the IT task both “ON” and “OFF” their typical dopaminergic medications, and compared to healthy age-matched control participants. These experiments
Participants
Fourteen patients with Parkinson’s disease (seven men and seven women) with an average age of 69.64 (S.D.=9.34, range=56–86 years), and 12 healthy control participants (four men and eight women) with an average age of 68.08 (S.D.=9.70, range=55–81 years) participated in this study. This between-group difference was not significant. In order to account for the possibility that group differences on IT were the result of group differences in IQ (e.g. due to non-random sampling), baseline cognitive
Results and discussion
IT ranged from 123.64 to 274.55 ms (M=169.35 ms, S.D.=44.54 ms) among PD patients, and from 61.82 to 170.91 ms (M=105.15 ms, S.D.=25.83 ms) among age-matched controls. Given the substantial difference between the standard deviations of these two groups, Levene’s test for homogeneity of variance was employed prior to assessing mean differences. This difference was found to be significant, F(1,24)=4.45, P<0.05, and so Mann–Whitney’s U-test was used to compare the group means. This test demonstrated
Participants
Twenty participants with Parkinson’s disease (13 men and 7 women) with an average age of 64.50 (S.D.=10.88, range=40–79) and 20 healthy control participants (6 men and 14 women) with an average age of 62.65 (S.D.=12.02, range=33–81) participated in the study. This between-group difference was not significant. Although these participants were drawn from the same sampling frame as the participants in the first study, this sample was completely orthogonal from the sample obtained in the first
Results and discussion
In the “OFF” condition (i.e. when medications are not effectively controlling PD symptoms), IT ranged from 80.00 to 240.00 ms (M=144.45 ms, S.D.=51.51 ms) within the PD group, and from 70.91 to 170.91 ms (M=101.71 ms, S.D.=27.34 ms) within the age-matched control group. In the “ON” condition (i.e. when medications are effectively controlling PD symptoms), IT ranged from 70.91 to 220.00 ms (M=139.55 ms, S.D.=51.23 ms) within the PD group, and from 61.82 to 174.55 ms (M=107.85 ms, S.D.=35.89 ms) within the
General discussion
Individuals with Parkinson’s disease have been demonstrated to show significant deficits in both simple reaction time, and cognitively non-complex choice RT (Gauntlett-Gilbert & Brown, 1998) suggesting a deficit related to some stage of processing prior to movement initiation. This deficit could, however, be related to the time required to perceive the input (i.e. processing information received from sensory organs); to the time required for planning a motor response and transmitting the output
Acknowledgements
This research was supported by grants from the Parkinson’s Foundation, and from the Natural Sciences and Engineering Research Council. The authors would also like to thank two anonymous reviewers for their helpful suggestions on an early draft of the manuscript.
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