Visual Hallucinations in Parkinson's Disease: a Hierarchy of Impairments Involving Perception, Source Monitoring and Reasoning

Research Article

Austin J Psychiatry Behav Sci. 2014;1(6): 1031.

Visual Hallucinations in Parkinson's Disease: a Hierarchy of Impairments Involving Perception, Source Monitoring and Reasoning

Edelstyn NMJ1*, Drakeford JL2 and Ellis SJ3

1School of Psychology, Keele University, UK

2School of Psychology, Staffordshire University, UK

3University Hospital of North Staffordshire, UK

*Corresponding author: Nicky Edelstyn, School of Psychology, Keele University, Keele, Staffordshire ST5 5BG, UK

Received: July 15, 2014; Accepted: August 12, 2014; Published: August 13, 2014


Up to 45% of patients with Parkinson's disease (PD) will develop visual hallucinations (VH) at some point in their illness. Although medication, depression, illness duration and ophthalmic abnormalities are identified as risk factors for VH-PD, specific perceptual and cognitive impairments may also play a role. The aim of this study was therefore to explore a hierarchy of low level perceptual processes, imagery and high level executive functions linked to reasoning in groups of VH and non VH PD.

This study investigated 18 patients with non dementing idiopathic PD. Nine patients had a history of VH. The VH and non VH PD groups were matched for demographic (age, gender), neuropsychological (premorbid and current levels of functioning) and clinical characteristics (disease duration, motor symptom severity, daily levodopa medication) apart from presence of VH in the index group. The VH-PD and non VH PD groups completed tests of bottom-up object processing and recognition, visual imagery, and top-down executive functions such as response inhibition, response suppression, source monitoring and spatial and probabilistic reasoning.

Compared to the non VH-PD group, VH-PD patients showed impairments in object perception and recognition impairments in cases when key identifying details were obscured. They also made more source misattribution errors, where self-generated images were misattributed to an external source. Finally, abnormalities in reasoning were evident. On the other hand, there were no differences between the VH-PD and non VH-PD groups on measures of visual perception using canonical views of objects, spatial perception, visual imagery, and other measures of executive function (initiation and suppression of responses, decision-making and self-monitoring).

The findings are discussed in relation to models of delusion and hallucination formation.

Keywords: Parkinson's disease; Visual hallucinations; Visual Perception; Visual Recognition; Source Memory; Reasoning


Hallucinations occur in the waking state and are defined as perceptions in the absence of environmental/external stimulation of the relevant sensory organ (see [1]. Surveys of psychiatric disturbance in Parkinson's disease (PD) report prevalence estimates of visual hallucinations (VH) between 8 to 45% [2-4]. The evolution of VH follows a progressive pattern, starting with vivid dreams, night terrors and nightmares, before gradually appearing during wakefulness and becoming increasingly more frequent. At first patients may retain insight into their VH; however their ominous nature is reflected in the VH becoming accompanied by paranoid and delusional ideation before leading to a permanent confusional state [5-9] Predisposing vulnerability factors include illness duration, medication, age, depression, sleep disturbance and cognitive decline [10]. Peripheral visual impairment also appears to be a contributory factor, as dim lighting i.e. use of scotopic vision appears to increase the frequency and duration of VH [11], in a manner similar to that described in Charles Bonnet Syndrome [12,13], a condition characterized by recurrent vivid VH in the presence of normal cognition and insight [14].

VH in PD develop within a multisystem neurodegenerative condition, which originate with the progressive loss of dopamine producing neurons in the substantia Ingra pars compact and ventral tegmental area [15]. This midbrain neuropathology in turn causes abnormal dopaminergic modulation of the striatum, leading to the hallmark motor signs of bradyphrenia, rigidity and tremor [16].

As a close functional relationship exists between the midbrain and neocortical areas including the prefrontal cortex [17] and the hippocampus (for a review, see [18], it is not surprising to find evidence in PD of deficits in both prefrontal-dependent functions which include planning, problem-solving, reasoning [19,20], response inhibition [21], working memory [22] and hippocampus-dependent primary memory processes that support delayed recall and the recollection of episodic details during recognition [21-23].

Although not traditionally included in the pathophysiological/ neuro pathological description of PD, several lines of evidence show abnormal dopaminergic modulation of the visual system is also present. Supporting evidence for this proposal is briefly outlined below.

First, macaque monkeys chronically treated with 1-methyl- 4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) as a model of PD, show morphological impairments in dopaminergic retinal neurons, particularly amacrine cells, the main neuronal subtype postsynaptic to dopaminergic cells. Additionally, electrical synapses among all classes of retinal cells, as well as chemical synapses between amacrine and rod bipolar cells, are deteriorated in parkinsonian monkeys. These results highlight that the scotopic visual pathway is severely impaired in the parkinsonian condition and provide a morphological basis for a number of abnormalities found in electrophysiological and psychophysical trials in PD patients and animal models [24].

Second, abnormal delays in visual evoked potentials (VEP) are reported in untreated de novo PD [25]. Furthermore, VEP abnormalities in PD were eliminated [25], or reduced in VH-PD [26], by the dopamine precursor levodopa.

Third, functional brain imaging reveals reduced activation of the lateral occipital cortex and extra striate temporal areas several seconds before image recognition in VH-PD compared to groups of non VH PD and healthy volunteers [27].

The central cognitive processes implicated in the development of VH in PD have not been extensively explored. Previous studies of hallucinations and delusions in other illnesses, such as schizophrenia for example, suggest that their presence is marked by a bias towards attributing an image which has been generated by oneself, to an external source, termed reality or source monitoring errors [28,29]. Source monitoring refers to the normal process by which perceived and imagined events are discriminated in memory. Memories originating from experienced events have more contextual, perceptual and meaningful information than memories derived from internally generated events such as dreams and fantasies [30,31]. However, if perceptual qualities of imagined events are unusually vivid, they may be more difficult to discriminate from perceived events. This may occur if reflective processes recruit an overabundance of perceptual processes during imagination. Another possible source of deficit in source monitoring is that healthy volunteers often refer to supporting memories and contextual information to substantiate their perceptions. A reduction in the amount of contextual information usually associated with perceived events or an increase in the contextual information associated with imagined events may produce deficits in reality monitoring [32]. If there is a disruption in the retrieval of contextual memories or the coding of these memories initially, the context of the input of the stimulus is likely to be reduced and the memory may be experienced as more isolated, foreign, and unreal to the individual. A deficit in the ability of an individual to access information during recall of real versus imagined events may similarly disrupt reality monitoring [31]. Another way in which internally derived imagination and externally derived memories are distinguished is through reasoning. Such processes include retrieving additional information from memory and considering if the target memory could have been perceived or self-generated given these other specific memories or general knowledge [33]. Garety and colleagues have found evidence of probabilistic reasoning biases in some hallucinating and deluded patients [34,35]. These biases were a tendency to make decisions on the basis of very little information (jumping to conclusions) and to express high levels of certainty (over-confidence). They also were more responsive to disconfirming information than were non psychotic controls, changing their decisions more rapidly. The material in the studies was neutral (concerning judgments about jars of colored beads), in a deliberate attempt to investigate judgments that were impersonal or emotionally loaded [36]. Were the first to investigate source monitoring in 22 VH-PD, 22 non VH-PD patients and 22 healthy controls. Their study revealed that VH-PD is marked by dissociation between (deficient) source monitoring, visual perception and (intact) visual imagery, spatial perception and imagery. These findings suggest that VH in PD could stem from a combination of faulty perceptual processing of environmental events/stimuli, and reduced reliance on contextual recollection during source monitoring.

Charles Bonnet Syndrome shows that vivid VHs can be precipitated by sensory deprivation alone. And it may be the case that abnormal dopamine in the visual pathway in PD may also contribute to the qualitative nature of the type of VH experienced in PD. However, unlike cases of Charles Bonnet Syndrome, VH-PD is marked by cognitive impairment and diminished insight [37].

The studies reviewed so far suggest that abnormalities in the processing of images, beginning at the level of the retina and continuing up to occipito-temporal areas may be risk factors for VH in PD. So that degraded images present the visual system with anomalous images which can be misinterpreted. However, visual perceptual and visual recognition impairments are only part of the story. Studies of other psychopathologies, such as the Capgras delusion, suggest that impairments in prefrontal-dependent executive functions linked to abnormal reasoning also play a critical role. Capgras delusion is characterized by the abnormal belief that one or a small number of highly significant or familiar others have been replaced by imposters who bear a close physical similarity to the original/s [38]. The delusion can be part of a broader psychotic illness such as paranoid schizophrenia or schizoaffective disorder, but can also develop in isolation within the context of a neurological condition, such as stroke or head injury [38]. Functional and structural imaging of a number of these cases shows Capgras delusion to be associated with the presence of focal right hemisphere lesions involving both prefrontal and parietal/temporal neocortical areas [39-41]. The co-occurrence of anterior and posterior lesions, together with evidence of executive and perceptual impairments in Capgras delusion (for example [40], is consistent with the proposal that abnormal prefrontal-dependent reasoning or reality testing styles or bias' fails to discount well-established perceptual disturbances [42].

In sum, these separate lines of evidence suggest that VH in PD may arise out of a hierarchy of perceptual and cognitive processing abnormalities which include a bottom-up retinal and posterior cortical impairment in the visual encoding and perception of fine detail which leads to the misidentification of objects in the environment; second, an increased propensity to believe that internally generated mental images are real items occurring in the environment; and finally, a top-down/anterior cortical reasoning deficiency in which VH-PD patients fail to eliminate an irrelevant hypothesis and are more likely to omit one or more appropriate hypotheses from consideration. The model is illustrated in Figure 1.