Are patients with Parkinson's disease blind to blindsight?

Abstract

In Parkinson's disease, visual dysfunction is prominent. Visual hallucinations can be a major hallmark of late stage disease, but numerous visual deficits also occur in early stage Parkinson's disease. Specific retinopathy, deficits in the primary visual pathway and the secondary ventral and dorsal pathways, as well as dysfunction of the attention pathways have all been posited as causes of hallucinations in Parkinson's disease. We present data from patients with Parkinson's disease that contrast with a known neuro-ophthalmological syndrome, termed 'blindsight'. In this syndrome, there is an absence of conscious object identification, but preserved 'guess' of the location of a stimulus, preserved reflexive saccades and motion perception and preserved autonomical and expressive reactions to negative emotional facial expressions. We propose that patients with Parkinson's disease have the converse of blindsight, being 'blind to blindsight'. As such they preserve conscious vision, but show erroneous 'guess' localization of visual stimuli, poor saccades and motion perception, and poor emotional face perception with blunted autonomic reaction. Although a large data set on these deficits in Parkinson's disease has been accumulated, consolidation into one specific syndrome has not been proposed. Focusing on neuropathological and physiological data from two phylogenetically old and subconscious pathways, the retino-colliculo-thalamo-amygdala and the retino-geniculo-extrastriate pathways, we propose that aberrant function of these systems, including pathologically inhibited superior colliculus activity, deficient corollary discharges to the frontal eye fields, dysfunctional pulvinar, claustrum and amygdaloid subnuclei of the amygdala, the latter progressively burdened with Lewy bodies, underlie this syndrome. These network impairments are further corroborated by the concept of the 'silent amygdala'. Functionally being 'blind to blindsight' may facilitate the highly distinctive 'presence' or 'passage' hallucinations of Parkinson's disease and can help to explain handicaps in driving capacities and dysfunctional 'theory of mind'. We propose this synthesis to prompt refined neuropathological and neuroimaging studies on the pivotal nuclei in these pathways in order to better understand the networks underpinning this newly conceptualized syndrome in Parkinson's disease.

Keywords: Parkinson’s disease; blindsight; hallucinations; pre-emptive perception; superior colliculus.

Figure 1

Schematic representation of the visual pathways. Beside the conscious geniculo-striate pathway (dashed lines), there are two subconscious visual pathways that do not pass through V1: the RCTA (dashed/dotted lines) and the RGES (closely spaced dotted lines). Of note, the discussed extension of the RCTA to the amygdala is not represented in the figure. For further explanations see text from Danckert and Rossetti (2005); with permission. LGN = lateral geniculate nucleus; SC = superior colliculus.

Figure 2

Cortical and subcortical pathways for vision and emotion. (a) The primary visual pathway (shown by thick arrows) originates from the retina and projects to the primary V1 in the occipital lobe via an intermediate station in LGN of Th. From V1, visual information reaches the extrastriate cortex along the ventral (occipitotemporal) and the dorsal (occipitoparietal) stream. However, a minority of fibres originating from the retina take a secondary route (shown by thin arrows) and reach both SC and Pulv. These two subcortical sites are connected and also send direct projections to the extrastriate visual cortex, bypassing V1. Another V1-independent visual pathway consists of the direct projections between the superior colliculus and LGN that, in turn, send efferents to extrastriate cortices in the dorsal stream. (b) The ‘emotion system' includes several cortical and subcortical areas. Among the subcortical structures are AMG and SI (shown in green), which are buried deeply in the temporal lobe and in the basal forebrain, respectively, NA in the basal ganglia (shown in green) and brainstem nuclei (shown in yellow), such as PAG and LC. Among cortical areas (shown in red) are OFC and ACC. The visual and emotional systems are extensively interconnected, especially at the subcortical level, where the superior colliculus is connected to the amygdala via the pulvinar. Direct connections also exist between subcortical and cortical emotion regions (for example, between the amygdala and OFC or ACC), between subcortical structures for emotions and cortical visual areas (for example, between the amygdala and temporal cortex) (not shown) and between brainstem nuclei and the cortex via diffuse projections (shown only from the LC). Grey arrows indicate connections within the emotion system. ACC = anterior cingulate cortex; AMG = amygdala; LC = Locus coeruleus; LGN = lateral geniculate nucleus; NA = nucleus accumbens; OFC = orbitofrontal cortex; PAG = periaqueductal grey; Pulv = pulvinar; SC = superior colliculus; SI = substantia innominata; Th = thalamus; V1 = primary visual cortex.