Brain Networks Involved in Sensory Perception in Parkinson's Disease: A Scoping Review

Abstract

Parkinson's Disease (PD) has historically been considered a disorder of motor dysfunction. However, a growing number of studies have demonstrated sensory abnormalities in PD across the modalities of proprioceptive, tactile, visual, auditory and temporal perception. A better understanding of these may inform future drug and neuromodulation therapy. We analysed these studies using a scoping review. In total, 101 studies comprising 2853 human participants (88 studies) and 125 animals (13 studies), published between 1982 and 2022, were included. These highlighted the importance of the basal ganglia in sensory perception across all modalities, with an additional role for the integration of multiple simultaneous sensation types. Numerous studies concluded that sensory abnormalities in PD result from increased noise in the basal ganglia and increased neuronal receptive field size. There is evidence that sensory changes in PD and impaired sensorimotor integration may contribute to motor abnormalities.

Keywords: Parkinson’s; basal ganglia; brain network; functional magnetic imaging; microelectrode; positron emission tomography; sensorimotor; sensory.

Figure 1

PRISMA scheme of reviewed literature.

Figure 2

Breakdown of the numbers of studies extracted between disease state, animal or human cohort and sensory modality.

Figure 3

Breakdown brain activation interrogation modalities. fMRI = functional magnetic resonance imaging, PET = positron emission tomography, TMS = transcranial magnetic stimulation, EEG = electroencephalogram, ERP = event related potential.

Figure 4

Brain areas involved in temporal processing; the green shading denotes areas found to be involved in healthy controls (ACC = 1 study, SMA = 4 studies, pre-SMA = 3 studies, temporal gyri = 3 studies, PPC = 3 studies, putamen = 4 studies) and the red outline denotes areas found to function abnormally in patients with Parkinson’s disease (DLPFC = 1 study, SMA = 1 study, precuneus = 1 study, putamen = 1 study). This summarises findings from 13 human studies. PPC = posterior parietal cortex, SMA = supplementary motor area, DLPFC = dorsolateral prefrontal cortex, SMA = supplementary motor area, pre-SMA = pre supplementary motor area, ACC = anterior cingulate cortex.

Figure 5

Brain areas involved in auditory processing; the green shading denotes areas found to be involved in healthy controls (ACC = 2 studies, superior temporal gyrus = 2 studies, putamen = 1 study, globus pallidus = 1 study, SN = 1 study, caudate = 1 study) and the red outline denotes areas found to function abnormally in patients with Parkinson’s disease (superior temporal gyrus = 3 studies, globus pallidus = 1 study). This summarises findings from 7 human studies and 2 animal studies. ACC = anterior cingulate cortex. GPi = globus pallidus internal, GPe = globus pallidus externa.

Figure 6

Brain areas involved in visual processing; the green shading denotes areas found to be involved in healthy controls (primary visual cortex = 2 studies, caudate = 2 studies, putamen = 1 study, substantia nigra = 2 studies, globus pallidus = 1 study) and the red outline denotes areas found to function abnormally in patients with Parkinson’s disease (primary visual cortex = 4 studies, retina = 4 studies, globus pallidus = 1 study). This summarises findings from 8 human studies and 2 animal studies. GPi = globus pallidus interna, GPe = globus pallidus externa.terior cingulate cortex. GPi = globus pallidus internal, GPe = globus pallidus externa.

Figure 7

Brain areas involved in tactile processing; the green shading denotes areas found to be involved in healthy controls (S1 = 7 studies, IPL = 1 study, caudate = 3 studies, substantia nigra = 2 studies, globus pallidus = 2 studies) and the red outline denotes areas found to function abnormally in patients with Parkinson’s disease (S1 = 3 studies, parietal lobe = 2 studies, premotor area = 2 studies, globus pallidus = 1 study). This summarises findings from 7 human and 4 animal studies. IPL = inferior parietal lobe, S1 = primary somatosensory cortex, GPi = globus pallidus interna, GPe = globus pallidus externa.

Figure 8

Brain areas involved in proprioceptive processing; the green shading denotes areas found to be involved in healthy controls (S1 = 2 studies, S2 = 1 study, M1 = 1 study, SMA = 1 study, putamen = 1 study, globus pallidus = 3 studies, STN = 2 studies) and the red shading denotes areas found to function abnormally in patients with Parkinson’s disease (S1 = 2 studies, S2 = 1 study, M1 = 1 study, lateral premotor = 1 study, posterior cingulate = 1 study, STN = 1 study, globus pallidus = 1 study, putamen = 1 study). This summarises findings from 12 human and 2 animal studies. S2 = secondary somatosensory cortex, S1 = primary somatosensory cortex, M1 = primary motor cortex, SMA = supplementary motor area, STN = subthalamic nucleus, GPi = globus pallidus interna, GPe = globus pallidus externa.