fMRI of global visual perception in simultanagnosia

doi:10.1016/j.neuropsychologia.2008.10.025

Neuropsychologia

Volume 47, Issue 4, March 2009, Pages 1173-1177

https://doi.org/10.1016/j.neuropsychologia.2008.10.025 Get rights and content

Abstract

The integration of visual elements into global perception seems to be implemented separately to single object perception. This assumption is supported by the existence of patients with simultanagnosia who can identify single objects but are incapable of integrating multiple visual items. We investigated a case of simultanagnosia due to posterior cortical atrophy without structural brain damage who demonstrated an incomplete simultanagnosia. The patient successfully recognized a global stimulus in one trial but failed to do so just a few seconds later. Using event-related fMRI, we contrasted post hoc selected trials of successful global perception with trials of global recognition failure. We found circumscribed clusters of activity at the right and left primary intermediate sulci and a bilateral cluster at the ventral precuneus. The integration of multiple visual elements resulting in a conscious perception of their gestalt seems to rely on these bilateral structures in the human lateral and medial inferior parietal cortex.

Introduction

Simultanagnosia is a rare neurological disorder characterized by the inability to visually perceive more than one object at a time although single object perception is unimpaired (Wolpert, 1924). Patients’ behaviour suggests a dissociation between the integration of multiple objects into a global gestalt and single object recognition. This is not to say that single object recognition and integration of multiple objects are not closely related and interconnected processes. However, structural damage and/or metabolic deficits in these patients affect specialized neural substrates and functions that are vital for the integration of multiple objects but not for single object recognition.

Simultanagnosia has been observed after ischemic stroke or haemorrhage (Bálint, 1909; Clavagnier, Fruhmann Berger, Klockgether, Moskau, & Karnath, 2006; Coslett & Saffran, 1991; Friedman-Hill, Robertson, & Treisman, 1995; Karnath, Ferber, Rorden, & Driver, 2000; Luria, 1959; Rizzo & Vecera, 2002; Wolpert, 1924) and with neurodegenerative disease, causing posterior cortical atrophy (PCA) (Tang-Wai et al., 2004). Patients typically suffer from extensive bilateral damage or hypometabolism of the parieto-occipito-temporal cortices (Bálint, 1909; Coslett & Saffran, 1991; Friedman-Hill et al., 1995; Karnath et al., 2000; Nestor, Caine, Fryer, Clarke, & Hodges, 2003; Rizzo & Vecera, 2002). To date, precise analyses of the functional anatomy of simultanagnosia were hindered by the small number of patients and the large extent of individual brain damage. Here, we studied a patient with simultanagnosia due to PCA who demonstrated residual global recognition shifting between intact performance and failure of global gestalt perception on a short time scale. Her simultanagnosia was not the consequence of extensive structural damage due to stroke or trauma. Therefore, brain activation in the hypometabolic regions was, in principle, accessible by functional neuroimaging, although we did observe first signs of cortical atrophy. This situation allowed us to conduct an event-related fMRI experiment and analyze brain activation based on a post hoc selection of correct vs. failed perception of the global gestalt of visual stimuli. This intra-individual comparison – eliminating physical differences between the stimuli – allowed us to localize a specific network involved in global perception in this patient, and presumably also present in other humans.

Section snippets

Patient RJ

RJ, a 59-year-old, right-handed woman, was admitted to our department complaining about “visual impairments”. She was severely impaired in reading whole sentences although she was able to read single words. During her clinical examination, she demonstrated a striking impairment in the recognition of the global level of Navon letters presented on a sheet of paper (Navon, 2003). Her responses were considerably delayed and/or incorrect. In contrast, she immediately identified respective local

Results

The psychophysical measurement of global recognition revealed a clear dissociation of accuracy (local: 90% correct; global: 50% correct; χ² = 22.617, p < 0.001), indicating severe impairment of the integration of local elements into a global gestalt. Nevertheless, in half of the trials the patient immediately recognized the large letter in the global condition, a performance that is well above chance level.

During functional imaging she successfully identified 44 global letters. The errors consisted

Discussion

Previous case reports of stroke patients with simultanagnosia pointed to the posterior parietal cortex as the neural correlate of the disorder. However, cortical damage or hypometabolism in these patients was typically widespread (Bálint, 1909; Coslett & Saffran, 1991; Friedman-Hill et al., 1995, Karnath et al., 2000, Nestor et al., 2003; Rizzo & Vecera, 2002). Lesion group studies that would allow more precise analyses of the functional anatomy (see Karnath & Rorden, 2004) were hindered to

Acknowledgments

This work was supported by the Bundesministerium für Bildung und Forschung (BMBF-Verbund “Visuo-spatial cognition” 01GW0654). We are deeply grateful to RJ for her outstanding patience and motivation.

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NotefMRI of global visual perception in simultanagnosia

Abstract

Introduction

Section snippets

Patient RJ

Results

Discussion

Acknowledgments

Neuropsychologia

Neuroimage

Acta Psychologica (Amsterdam)

Psychiatry Research

Neuroimage

Seelenlähmung des “Schauens”, optische Ataxie, räumliche Störung der Aufmerksamkeit

Monatsschrift fur Psychiatrie und Neurologie

Restricted ocular exploration does not seem to explain simultanagnosia

Neuropsychologia

Control of goal-directed and stimulus-driven attention in the brain

Nature Reviews. Neuroscience

Simultanagnosia: To see but not two see

Brain

Visual perception without awareness in a patient with posterior cortical atrophy: Impaired explicit but not implicit processing of global information

Journal of International Neuropsychological Society

Neural mechanisms involved in the processing of global and local aspects of hierarchically organized visual stimuli

Brain

Parietal contributions to visual feature binding: Evidence from a patient with bilateral lesions

Science

Assessing the significance of focal activations using their spatial extent

Human Brain Mapping

Note
fMRI of global visual perception in simultanagnosia