Intrinsic motivation in patients with Parkinson\u2019s disease: a neuropsychological investigation of curiosity using dopamine transporter imaging

Yayoi Shigemune,Toru Baba,Nobuhito Abe,Atsushi Takeda,Iori Kawasaki,Akira Midorikawa

doi:10.1007/s10072-020-04968-4

Yayoi Shigemune, Toru Baba + Show 4 more

Open Access

https://doi.org/10.1007/s10072-020-04968-4

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Abstract

Both intrinsic and extrinsic motivation are believed to involve brain regions that are innervated by the dopaminergic pathway. Although dopaminergic neurons in the midbrain deteriorate in Parkinson’s disease (PD), it remains unclear whether intrinsic motivation is impaired in PD patients. To address this issue, we investigated intrinsic motivation in PD patients using a task designed to assess the “Pandora effect,” which constitutes a curiosity for resolving uncertainty, even if this curiosity is likely to result in negative consequences. Twenty-seven PD patients and 27 age-matched healthy controls (HCs) completed a curiosity task in which they were required to decide either to view or skip negative pictures (e.g., snakes, spiders) and an examination battery that included the Mini-Mental State Examination, a verbal fluency test, the Trail Making Test, 10-word recall tests, and questionnaires for behavioral inhibition/activation and depression. DaTSCAN images to assess the distribution of dopamine transporters in the striatum were acquired only from PD patients. The results revealed that PD patients, relative to the HCs, viewed the pictures less frequently under both the certain and uncertain conditions. However, both the PD patients and HCs viewed the pictures at a higher frequency under the uncertain condition than under the certain condition. In the PD patients, the proportion of pictures viewed under the certain condition was positively correlated with the distribution of dopamine transporters in the striatum. These results suggest that despite the overall decreasing level of interest in viewing negative pictures, the motivation to resolve uncertainty is relatively intact in PD patients.

Highlights

The major neuropathological feature of Parkinson’s disease (PD) is the degeneration of dopaminergic neurons in the Sendai-Nishitaga Hospital, Sendai, Japan 4 Department of Psychology, Faculty of Letters, Chuo University, Tokyo, Japan 5 Department of Neurology, National Hospital OrganizationSendai-Nishitaga Hospital, Sendai, Japan 6 Kokoro Research Center, Kyoto University, Kyoto, Japan substantia nigra and ventral tegmental area of the midbrain [1, 2]
Despite accumulated evidence indicating that intrinsic and extrinsic motivation share a common neural basis, it remains unclear whether intrinsic motivation deteriorates in PD patients accompanied by the loss of striatal dopaminergic transmission. We investigated this unexplained issue using 123Iioflupane single-photon emission computed tomography (SPECT) (DaTSCAN) images to assess the distribution of dopamine transporters in the striatum, combined with a task designed to assess the “Pandora effect,” which constitutes a curiosity for resolving uncertainty, even if this curiosity is likely to result in negative consequences [15]
Two-sample t tests showed no significant differences in the Mini-Mental State Examination (MMSE) (t(52) = − 0.58, p = 0.56, r = 0.08), phonemic verbal fluency (VF) test (t(52) = − 1.86, p = 0.07, r = 0.25), semantic VF test (t(52) = − 1.55, p = 0.13, r = 0.21), 10-word recall test of the Alzheimer’s Disease Assessment Scale (ADAS) (t(52) = − 0.06, p = 0.95, r = 0.01), or BIS (t(52) = − 1.76, p = 0.08, r = 0.24) scores, but significant differences in Trail Making Test (TMT) (PD patients > healthy controls (HCs)) (t(38.7) = 3.17, p < 0.01, r = 0.40), BAS

Summary

Introduction

The major neuropathological feature of Parkinson’s disease (PD) is the degeneration of dopaminergic neurons in the Sendai-Nishitaga Hospital, Sendai, Japan 4 Department of Psychology, Faculty of Letters, Chuo University, Tokyo, Japan 5 Department of Neurology, National Hospital Organization. Sendai-Nishitaga Hospital, Sendai, Japan 6 Kokoro Research Center, Kyoto University, Kyoto, Japan substantia nigra and ventral tegmental area of the midbrain [1, 2]. The dopaminergic neurons in the substantia nigra and ventral tegmental area project to the striatum, and these dopaminergic projections are included in the reward circuit [3]. Striatal dopaminergic transmissions deteriorate in PD patients [4], and these localized impairments in the dopaminergic reward pathway induce abnormal rewardrelated activation and processing among PD patients [5]

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