Impaired serial ordering in nondemented patients with mild Parkinson's disease.

Jinghong Ma,Haiqiang Zou,Zheng Ye,Piu Chan,Shaoyang Ma,Yizhi Zhang,Stephen D Ginsberg

doi:10.1371/journal.pone.0197489

Abstract

The ability to arrange thoughts and actions in an appropriate serial order (the problem of serial order) is essential to complex behaviors such as language, reasoning and cognitive planning. Patients with Parkinson’s disease (PD) perform poorly in tasks that rely on the successful rearrangement of working memory representations. We hypothesized that serial ordering is impaired in nondemented patients with mild PD. We recruited 49 patients with mild idiopathic PD (Hoehn and Yahr Scale 1–2.5) and 51 matched healthy adults. Nineteen patients had normal global cognition (PD-NC, Montreal Cognitive Assessment, MoCA≥26/30) and thirty patients had mild cognitive impairment (PD-MCI, 21≤MoCA≤25). All participants underwent three working memory assessments: two experimental tests that require reordering random digits following a particular rule (adaptive digit ordering test and digit span backward test) and a control test that requires maintaining but no reordering (digit span forward test). PD-NC and PD-MCI patients performed significantly worse (with lower test scores and larger ordering costs) than healthy controls in both digit ordering and backward tests, although they performed normally in the forward test. The ordering cost increased as a function of age across groups, indicating an aging-related decline in the ability of serial ordering. However, individual patients’ task performances were not correlated with their severity or duration of motor symptoms, or daily exposure to dopaminergic drugs. These results suggested that serial ordering deficits exist in early stages of PD, prior to subtle changes in global cognition and in parallel with motor symptoms.

Highlights

In humans, the ability to arrange thoughts and actions in an appropriate serial order is essential to complex behaviors such as language production and cognitive planning
We examined behavioral performance of serial ordering tests in Parkinson’s disease (PD) patients with mild motor symptoms (Hoehn and Yahr Scale, HY, 1–2.5) and with normal global cognition (Montreal Cognitive Assessment, MoCA!26/30) or mild cognitive impairment (21 MoCA 25)
PD-NC patients scored higher than PD-MCI patients in the DOT-A (t = 2.50, p = 0.016). It means serial ordering was impaired in PD-NC patients regardless of the ordering rule and became worse in PD-MCI patients

Summary

Introduction

The ability to arrange thoughts and actions in an appropriate serial order is essential to complex behaviors such as language production (e.g. which information to convey first) and cognitive planning (e.g. which subgoal to achieve first). Medicated PD patients had difficulties in finding the temporal order of letters which were presented in loop [2] or that of public events which were presented in a scrambled order [3]. They often failed to understand the temporal relation of events which were expressed out of chronological order [4, 5] or to organize a series of temporally related but randomly presented events to tell a sensible story [6, 7]. PD’s difficulties in rearranging events along the time axis have been linked with aberrant activations over the dorsolateral prefrontal cortex and striatum [4, 7]

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Results

Conclusion