Compensatory task-specific hypersensitivity in bilateral planum temporale and right superior temporal gyrus during auditory rhythm and omission processing in Parkinson\u2019s disease

Kjetil Vikene,Geir Olve Skeie,Karsten Specht

doi:10.1038/s41598-019-48791-0

Abstract

Persons with Parkinson’s disease have general timing deficits and have difficulties in rhythm discrimination tasks. The basal ganglia, a crucial part of Parkinson’s disease pathology, is believed to play an important role in rhythm and beat processing, with a possible modulation of basal ganglia activity by level of rhythmic complexity. As dysfunction in basal ganglia impacts function in other brain areas in Parkinson’s disease during temporal processing, investigating the neuronal basis for rhythm processing is important as it could shed light on the nature of basal ganglia dysfunction and compensatory mechanisms. We constructed an auditory beat-omission fMRI paradigm with two levels of rhythm complexity, to investigate if and where persons with Parkinson’s disease showed abnormal activation during rhythm and omission processing, and whether such activations were modulated by the level of rhythmic complexity. We found no effect of complexity, but found crucial group differences. For the processing of normal rhythm presentations, the Parkinson-group showed higher bilateral planum temporal activity, an area previously associated with the processing of complex patterns. For the omissions, the Parkinson-group showed higher activity in an area in the right superior temporal gyrus previously associated with detection of auditory omissions. We believe this shows a pattern of “hypersensitive” activity, indicative of task-specific, compensatory mechanisms in the processing of temporal auditory information in persons with Parkinson’s disease.

Highlights

Persons with Parkinson’s disease (PD) have general timing deficits[1,2], and perhaps as a particular manifestation of this, they have been found to have difficulties in rhythm discrimination tasks[3,4,5]
The main source of MMNs and auditory omissions has consistently been located in the intersection of the STG, PT and HG25–35, areas crucially involved in rhythm perception
We were interested in differences in activation of basal ganliga areas, superior temporal gyrus and planum temporale, as well as in areas in the superior temporal gyrus found to be activated by auditory omissions in previous studies

Summary

Introduction

Persons with Parkinson’s disease (PD) have general timing deficits[1,2], and perhaps as a particular manifestation of this, they have been found to have difficulties in rhythm discrimination tasks[3,4,5]. A difference between simple (isochronous or strongly metric), complex (non-isochronous, weakly metric) and non-metric rhythms is well established in both behavriousl, EEG/ERP and fMRI-studies perception[7,8,9,10,11], influenced to a large part by the work of Povel & Essens[12,13] Another rhythm framework posits that hierarchical beat position and position deviations are central features influencing our perception[14,15,16,17,18,19] and speak to how we process rhythmic complexity within a rhythm. We were interested in differences in activation of basal ganliga areas, superior temporal gyrus and planum temporale, as well as in areas in the superior temporal gyrus found to be activated by auditory omissions in previous studies

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