Brain Advance Access originally published online on September 15, 2009
Brain 2009 132(11):2980-2993; doi:10.1093/brain/awp223
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Impaired visual processing preceding image recognition in Parkinson's disease patients with visual hallucinations
1 Department of Neurology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands 2 Neuro Imaging Center (NIC) Groningen, University of Groningen, Groningen, The Netherlands 3 School of Behavioral and Cognitive Neurosciences, University of Groningen, Groningen, The Netherlands 4 Laboratory of Experimental Ophthalmology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
Correspondence to: Anne Marthe Meppelink, MD, Department of Neurology, University Medical Center Groningen, Hanzeplein 1, 9700 RB Groningen, The Netherlands E-mail: a.m.meppelink{at}neuro.umcg.nl
Impaired visual processing may play a role in the pathophysiology of visual hallucinations in Parkinson's disease. In order to study involved neuronal circuitry, we assessed cerebral activation patterns both before and during recognition of gradually revealed images in Parkinson's disease patients with visual hallucinations (PDwithVHs), Parkinson's disease patients without visual hallucinations (PDnonVHs) and healthy controls. We hypothesized that, before image recognition, PDwithVHs would show reduced bottom-up visual activation in occipital-temporal areas and increased (pre)frontal activation, reflecting increased top-down demand. Overshoot of the latter has been proposed to play a role in generating visual hallucinations. Nine non-demented PDwithVHs, 14 PDnonVHs and 13 healthy controls were scanned on a 3 Tesla magnetic resonance imaging scanner. Static images of animals and objects gradually appearing out of random visual noise were used in an event-related design paradigm. Analyses were time-locked on the moment of image recognition, indicated by the subjects’ button-press. Subjects were asked to press an additional button on a colour-changing fixation dot, to keep attention and motor action constant and to assess reaction times. Data pre-processing and statistical analysis were performed with statistical parametric mapping-5 software. Bilateral activation of the fusiform and lingual gyri was seen during image recognition in all groups (P < 0.001). Several seconds before image recognition, PDwithVHs showed reduced activation of the lateral occipital cortex, compared with both PDnonVHs and healthy controls. In addition, reduced activation of extrastriate temporal visual cortices was seen just before image recognition in PDwithVHs. The association between increased vulnerability for visual hallucintions in Parkinson's disease and impaired visual object processing in occipital and temporal extrastriate visual cortices supported the hypothesis of impaired bottom-up visual processing in PDwithVHs. Support for the hypothesized increased top-down frontal activation was not obtained. The finding of activation reductions in ventral/lateral visual association cortices in PDwithVHs before image recognition further helps to explain functional mechanisms underlying visual hallucinations in Parkinson's disease.
Key Words: fMRI; Parkinson's disease; visual hallucinations
Abbreviations: BDI, Beck depression inventory; CBS, Charles Bonnet syndrome; FAB, frontal assessment battery; FIR, finite impulse response; fMRI, functional magnetic resonance imaging; LEDD, Levodopa-equivalent daily dose; MMSE, Mini Mental State Examination; PDnonVH, Parkinson's disease patients without visual hallucinations; PDwithVH, Parkinson's disease patients with visual hallucinations; SPM, statistical parametric mapping; UPDRS, Unified Parkinson's Disease Rating Scale; VH, visual hallucinations
Received March 23, 2009. Revised July 14, 2009. Accepted July 15, 2009.