Pareidolia in Parkinson's disease without dementia: A positron emission tomography study

Highlights

• A test to evoke pareidolia was administered to 53 patients with PD without dementia and 24 healthy controls.

• The cerebral glucose metabolism was measured using FDG-PET.

• PD patients produced a greater number of pareidolias compared with the controls.

• The indices of pareidolias and visual hallucinations were correlated with hypometabolism in the bilateral temporo-parieto-occipital cortices and that in the left parietal cortex, respectively.

• A region associated with both pareidolias and visual hallucinations was found in the left parietal cortex.

Abstract

Background

Pareidolia, which is a particular type of complex visual illusion, has been reported to be a phenomenon analogous to visual hallucinations in patients with dementia with Lewy bodies. However, whether pareidolia is observed in Parkinson's disease (PD) or whether there are common underlying mechanisms of these two types of visual misperceptions remains to be elucidated.

Methods

A test to evoke pareidolia, the Pareidolia test, was administered to 53 patients with PD without dementia and 24 healthy controls. The regional cerebral metabolic rate of glucose was measured using 18F-fluorodeoxyglucose positron emission tomography in the PD patients.

Results

PD patients without dementia produced a greater number of pareidolic illusions compared with the controls. Pareidolia was observed in all of the patients having visual hallucinations as well as a subset of those without visual hallucinations. The number of pareidolic illusions was correlated with hypometabolism in the bilateral temporal, parietal and occipital cortices. The index of visual hallucinations was correlated with hypometabolism in the left parietal cortex. A region associated with both pareidolia and visual hallucinations was found in the left parietal lobe.

Conclusions

Our study suggests that PD patients without dementia experience pareidolia more frequently than healthy controls and that posterior cortical dysfunction could be a common neural mechanism of pareidolia and visual hallucinations. Pareidolia could represent subclinical hallucinations or a predisposition to visual hallucinations in Lewy body disease.

Introduction

Visual misperceptions, i.e., visual hallucinations and illusions, are among the behavioral symptoms that distinguish Lewy body diseases (LBD) from other movement and cognitive disorders. Visual hallucinations have been reported to be present in approximately 80% of patients with dementia with Lewy bodies (DLB) [1], [2], in more than 50% of patients with Parkinson's disease (PD) with dementia [1], [3] and in 10% of patients with PD without dementia [1], [3], [4]. Visual illusions have been observed in 30–50% of patients with DLB [5], in 58% of patients with PD with dementia [3] and in 6–19% of patients with PD without dementia [3], [4]. These two different types of visual misperceptions have been grouped under the term PD-associated psychosis [6], in which visual illusions have been categorized as minor hallucinations [7]. However, there have been few empirical studies addressing the common underlying mechanisms of visual illusions and visual hallucinations.

The earliest clinical observations documented the frequent comorbidity of visual hallucinations with sleep-wake disorders, leading to the hypothesis that endogenous imagery produced during dreaming is the source of hallucinatory images [8], [9]. In addition, there is abundant clinical evidence supporting the hypothesis linking visual hallucinations with visual deficits, which were first described a hundred years ago [8], [10]. More recently, neuropsychological studies demonstrated the contribution of attention deficit to the emergence of visual hallucinations [11], [12]. These hypotheses have been integrated in recent neurobiological models of visual hallucinations in LBD, in which sleep disturbance/dream image intrusion is considered to arise from lesions in the brainstem and forebrain cholinergic and/or monoaminergic systems, whereas visual deficits are suggested to be associated with temporo-occipital cortical lesions [9]. Attention deficits have been attributed to disruptions of the cholinergic projections to the fronto-temporal cortices or the hypofunction of the dorsal attention network consisting of the dorsolateral prefrontal and posterior parietal cortices [11], [12].

In our previous studies, we devised the Pareidolia test, a tool evoking pareidolia, which is a complex visual illusion involving ambiguous forms that are perceived as meaningful objects. We found that patients with DLB experienced pareidolia more frequently than patients with Alzheimer's disease (AD) or healthy controls [13], [14]. Visual hallucinations and pareidolia in DLB were phenomenologically similar, with humans and animals being the most common themes. In addition, both conditions were improved by treatment with cholinesterase inhibitors [13], [14], [15], [16]. These findings suggest that visual hallucinations and pareidolia share underlying mechanisms in DLB. Pareidolia was observed not only in patients with DLB who had visual hallucinations but also those who did not [13], suggesting that pareidolia might represent a subclinical hallucination or a predisposition to visual hallucinations. Based on these findings, we predicted that pareidolia would be observed in a subset of PD patients without dementia or frank psychosis and that both visual hallucinations and pareidolia would be associated with dysfunction in similar brain regions, specifically temporo-occipital or fronto-parietal cortices. In this study, we tested this hypothesis using the Pareidolia test and 18F-fluorodeoxyglucose positron emission tomography (FDG-PET).