The neural correlates of topographical disorientation-a lesion analysis study.
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SUBMITTER: Blondiaux E
PROVIDER: S-EPMC10863913 | biostudies-literature | 2024 Feb
REPOSITORIES: biostudies-literature
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The neural correlates of topographical disorientation-a lesion analysis study.
Blondiaux Eva E Diamantaras Andreas A Schumacher Rahel R Blanke Olaf O Müri René R Heydrich Lukas L
Annals of clinical and translational neurology 20240117 2
Topographical disorientation refers to the selective inability to orient oneself in familiar surroundings. However, to date its neural correlates remain poorly understood. Here we use quantitative lesion analysis and a lesion network mapping approach in order to investigate seven patients with topographical disorientation. Our findings link not only the posterior parahippocampal gyrus (PHG) and retrosplenial cortex but also the lingual gyrus, the precuneus and the fusiform gyrus to topographical ...[more]
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Project description:IntroductionTopographical disorientation is defined as the inability to recognize familiar or unfamiliar environments. While its slowly progressive development is a common feature of neurodegenerative processes like Alzheimer's dementia, acute presentations are less frequent and mostly caused by strategic lesions within the cerebral navigation network. Depending on the lesion site, topographical disorientation can originate from deficits in landmark recognition and utilization for route planning (egocentric navigation deficit), or disturbance of an overarching cognitive map of the spatial environment (allocentric navigation deficit). However, objective measurements of spatial navigation performance over time are largely missing in patients with topographical disorientation.MethodsWe here report a 55-year-old patient with acute topographical disorientation as the single symptom of right-sided hippocampal hemorrhage and present quantitative gaze-monitoring head camera-based analyses of his path-finding strategy and visual exploration behavior in a real space navigation paradigm.ResultsThe patient exhibited severe allocentric and also egocentric navigation deficits during the acute phase, shown by higher error rates at finding target items. In addition, he showed a more extensive use of search saccades toward, and fixations on, landmarks that could potentially serve as spatial cues. These deficits had been completely compensated for after four months, when the patient performed unremarkably in the real space navigation task, and used even more strongly allocentric path optimization strategies than age-matched controls.ConclusionsThis case report highlights the integral function and right-sided dominance of the hippocampal formation in the cerebral navigation network in humans. It shows that the cognitive map can be restored completely despite a residual hippocampal lesion, which illustrates the enormous plasticity of the cerebral navigation network in humans.
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Project description:Neuropsychological studies on acquired topographical disorientation have provided useful insights into the contribution of different brain regions to human navigation. However, little is known about the possibility to restore navigational skills after brain damage. Here we describe the case of No Longer Lost (NLL), a 49-year-old man who complained of severe topographical disorientation following traumatic brain injury. Extensive neuropsychological evaluation at baseline revealed selective episodic memory deficits and topographical disorientation. NLL underwent 8-week imagery-based treatment (IBT) inspired by current cognitive models of human spatial navigation. After IBT, NLL improved topographical skills and episodic memory. From a clinical point of view, the present study describes a model-based intervention for topographical disorientation. From a theoretical point of view, it provides new insights into the cognitive models of human spatial navigation and straightforward evidence about common phylogenetic roots of brain mechanisms devoted to spatial navigation and memory.
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Project description:BackgroundThe neural and cognitive substrates of measures of orientation as used in clinical trials and examinations have not been comprehensively examined.MethodsWe studied 473 subjects diagnosed with mild cognitive impairment (MCI) and Alzheimer's disease (AD) at baseline in Alzheimer's Disease Neuroimaging Initiative. Regression analyses at baseline were conducted to find significant predictors of orientation score among cognitive, brain morphometry, and glucose metabolism measures. Mixed model longitudinal analysis was performed to examine consequences of orientation on functional decline, and Cox hazard models examined the risk of conversion to AD in the MCI group.ResultsIn MCI and AD subjects, orientation was predicted by poorer neurocognitive performance on immediate and delayed episodic memory and attention and processing speed. Among magnetic resonance imaging measures, orientation was predicted by entorhinal cortex thickness, hippocampal volume, and inferior temporal cortex thickness. Glucose metabolism in both middle-inferior temporal cortex and hippocampus were also predictive of orientation score. Functioning was significantly lower in disoriented subjects after 4 years of follow-up, and MCI patients who also were disoriented showed a higher rate of conversion to AD with a hazard ratio of 1.5.ConclusionsOrientation is associated with medial temporal lobe structure, temporal lobe glucose metabolism, and episodic memory function. In MCI individuals orientation was a risk factor for progression to AD, also associated with rapid functional decline and worse prognosis. Thus, orientation may serve as a surrogate for episodic memory in clinical examination. These results have direct implications for the use of orientation in MCI and AD clinical trials including ceiling effects in healthy controls and issues of redundancy with measures of memory, when both are used in composite scores.
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