Abstract
Background: Pareidolias are visual phenomena wherein ambiguous, abstract forms or shapes appear meaningful due to incorrect perception. In Parkinson's disease (PD), patients susceptible to visual hallucinations experience visuo-perceptual deficits in the form of pareidolias. Although pareidolias necessitate top-down modulation of visual processing, the cortical dynamics of internally generated perceptual priors on these visual misperceptions is unknown. Objectives: To study prestimulus-related electroencephalography (EEG) spectral and network abnormalities in PD patients experiencing pareidolias. Methods: Twenty-one PD in-patients and 10 age-matched controls were evaluated. Neuropsychological assessments included tests for cognition, attention, and executive functions. Pareidolias were quantified by using the "noise pareidolia test" with simultaneous EEG recording. The PD patients were subdivided into two groups-those with high pareidolia counts (n = 10) and those without (n = 11). The EEG was analyzed 1000 msec before stimulus presentation in the spectral domain (theta, low-alpha, and high-alpha frequencies) with corresponding graph networks to evaluate network properties. Statistical analysis included analysis of variance and multiple regression to evaluate the differences. Results: The PD patients with high pareidolia counts were older with lower scores on neuropsychological tests. Their prestimulus EEG low-alpha band showed a tendency toward higher frontal activity (p = 0.07). Graph networks showed increased normalized clustering coefficient (p = 0.05) and lower frontal degree centrality (p = 0.005). These network indices correlated positively to patients' pareidolia scores. Discussion: We suggest that pareidolias in PD are a consequence of an abnormal top-down modulation of visual processing; they are defined by their frontal low-alpha spectral and network alterations in the prestimulus phase due to a dissonance between patients' internally generated mental processing with external stimuli. Impact statement Pareidolias in Parkinson's disease (PD) are considered to be promising early markers of visual hallucinations and an indicator of PD prognosis. In certain susceptible PD patients, pareidolias can be evoked and studied. Here, via electroencephalography, we aimed at understanding this visual phenomenon by studying how neural information is processed before stimulus presentation in such patients. Using spectral and graph network measures, we revealed how top-down modulated internally generated processes affect visual perception in patients with pareidolias. Our findings highlight how prestimulus network alterations in the frontal cortex shape poststimulus pareidolic manifestations in PD.
Highlights
Parkinson’s disease (PD) is predominantly a motor neurodegenerative disease, but those affected frequently show nonmotor symptoms of psychosis such as mood disorders, impulsivity, and hallucinations (Ffytche et al, 2017)
We suggest that pareidolias in PD are a consequence of an abnormal top–down modulation of visual processing; they are defined by their frontal low-alpha spectral and network alterations in the prestimulus phase due to a dissonance between patients’ internally generated mental processing with external stimuli
Pareidolias can be quantified by using the noise pareidolia test (NPT), a neuropsychological test wherein ambiguous patterns are presented to evoke illusionary responses in PD or dementia with Lewy body patients (Uchiyama et al, 2012, 2015)
Summary
Parkinson’s disease (PD) is predominantly a motor neurodegenerative disease, but those affected frequently show nonmotor symptoms of psychosis such as mood disorders, impulsivity, and hallucinations (Ffytche et al, 2017). VH are often preceded by minor hallucinations (Lenka et al, 2019) wherein patients develop misperceptions of inanimate forms, objects, or shapes (Ffytche et al, 2017) These visuo-perceptual deficits commonly occur in the form of ‘‘pareidolias’’—misperceptions of ambiguous shapes or forms that appear meaningful—and serve as precursors in identifying hallucinatory tendencies in PD patients (Uchiyama et al, 2015). Results: The PD patients with high pareidolia counts were older with lower scores on neuropsychological tests Their prestimulus EEG low-alpha band showed a tendency toward higher frontal activity ( p = 0.07). Discussion: We suggest that pareidolias in PD are a consequence of an abnormal top–down modulation of visual processing; they are defined by their frontal low-alpha spectral and network alterations in the prestimulus phase due to a dissonance between patients’ internally generated mental processing with external stimuli
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