Visual inspection time in Parkinson’s disease: deficits in early stages of cognitive processing

Abstract

Inspection time (IT) is a simple information processing paradigm dependent on a participant’s ability to identify physical properties of a stimulus presented for a specified time interval. In contrast with reaction time (RT) studies, the dependent variable of interest in IT is not related to the motoric speed with which the individual is able to respond, but rather the minimum presentation time necessary for participants to reliably identify physical properties of the stimulus. It is well documented that individuals with Parkinson’s disease (PD) experience significant impairment on tests of simple RT, but it is unclear whether such deficits can be interpreted as ‘pure’ slowness of information processing, or a delay in the selection and output of a motor response. In the first experiment described here, a sample of ‘optimally medicated’ PD patients was compared with an age-matched control group, on an IT task. Results of this experiment suggested that individuals with PD required significantly longer stimulus presentation times than healthy participants. The second experiment compared a sample of PD patients (tested both “ON” and “OFF” their typical dopaminergic medications), with an age-matched control group, on the same test of IT. Results again indicated a significant IT deficit in participants with PD, and suggested that these deficits do not significantly resolve with levodopa treatment. Overall, the results of these two experiments suggest that information processing deficits associated with PD are distinct from motor impairment. These findings are further discussed in terms of existing neurochemical models of information processing ability.

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.