Long-lasting topographical disorientation in new environments

Abstract

We describe the case of a young woman with long-lasting topographical disorientation following a haemorrhagic lesion of the right temporo-occipital region involving the hippocampus. She was unable to orient herself in novel environments and to perform learning spatial tasks both in real-world settings and laboratory conditions. Her ability to recall and navigate through known routes as well as to recognize familiar landmarks was preserved. Neuropsychological evaluation revealed a mild long-term memory deficit. A similar neuropsychological and experimental pattern was observed 8 years later (at the time of follow-up) when she showed a persistent topographical disorientation and a slight worsening of verbal and visuo-spatial long-term memory disorders. Her topographical disorientation was characterized by an impairment confined to the anterograde memory domain, a not frequent pattern reported in literature, in the absence of remote topographical memory disorders. The presence of a lesion localized in the right occipito-temporal region and hippocampus combined with the results observed in some experimental tasks could also contribute to the debate of the role of neural correlates involved in topographical spatial knowledge.

Introduction

Topographical disorientation (TD) is characterized by the inability to navigate through familiar or unfamiliar environments. Patients affected by this type of spatial disorder may not be able to recall familiar routes or to learn novel routes. In literature, different types of TD have been described and classified under two major categories [1], [2], [3], [4], [5]: topographical agnosia and topographical amnesia, a dichotomy that remains somewhat unclear.

Topographical agnosia (see for example, [6]) has been typically described as a perceptual difficulty to identify and recognize landmarks (places, buildings, landscapes, streets etc.).

Topographical amnesia has been reported in patients with intact visual and spatial perceptual ability whereas memory for landmarks is impaired (for a review, see [7], [8]).

Also the neuroanatomical correlates are a matter of debate. Spatial deficits including TD have been associated with lesions due to stroke, traumatic injury, surgical treatment for epilepsy, encephalitis or neoplasia (with some exceptions, as the single case described by Iaria and colleagues [9] of a congenital brain malformation involving the bilateral retro-Rolandic regions, the case reported by Turriziani and colleagues [10] of a severe bilateral hippocampus atrophy and the patient affected by focal Alzheimer disease recently described by Grossi and colleagues [11]). The brain regions classically involved in the different varieties of TD are the parietal lobe (generally in the right hemisphere), the dorsal occipital parietal pathway, the retrosplenial cortex, the medial temporal lobes [7], [12], [13]. More in detail, the contribution of the role of hippocampus in spatial processing has been emphasized by different neuropsychological studies [12], [13], [14], [15], [16], [17], [18], [19], [20], [21] and confirmed by some functional neuroimaging studies [22], [23], [24], [25], [26].

In 1999, Aguirre and D'Esposito [1], on the basis on behavioural and neuroanatomical findings, proposed a detailed TD taxonomy considering four different categories.

Patients affected by egocentric disorientation are able to perceive landmarks but show difficulty in representing the location of landmarks in respect to the self (for example, [27]). Usually, the deficit is consequent to bilateral or unilateral right posterior parietal lobe lesions.

Patients with heading disorientation are selectively impaired with respect to the direction to go from the landmarks they are able to recognize (for example, [28]). Lesions are localized into the retrospenial cortex–posterior cingulated (see also [29]).

A larger and well-studied group of cases with TD is that of patients affected by landmark agnosia, a deficit characterized by the inability to use salient environmental features for orientation [30], [31], [32], [33]. The lesions involve cortical areas specialized in topographical representation: bilateral or right medial occipito-temporal cortex, including fusiform, lingual and parahippocampal gyri.

All the above mentioned cases of TD are impaired both in familiar and novel environments. However, some cases of TD related only to novel environments have been reported and have been classified by Aguirre and D'Esposito as anterograde disorientation [10], [16], [34], [35]. The disturbance has mainly been attributed to a prevalent inability of learning spatial relationships by visual imagery and the critical lesion site was more frequently localized into the right hippocampus and parahippocampal areas.

As we can see, the different studies reported in literature suggest that TD is a complex multicomponent deficit and the specific role of distinct neuroanatomical areas is, in part, controversial.

In the present study, we report the case of R.G. who, when she was 22 years old, after a haemorrhagic lesion involving the right temporo-occipital region and the hippocampus, showed an impairment in memorizing environmental landmarks associated with an inability of recalling the location of different spatial landmarks, in the presence of a mild memory impairment. Furthermore, this case has provided us with the opportunity to perform a longitudinal evaluation of her clinical and neuropsychological deficits: 10 years after the stroke, the patient (who was 32 years old) revealed a persistent impairment of the ability to find the way in new environments in the context of a long-term memory deficit.

We believe our patient represents an interesting example of a long-lasting anterograde topographical amnesia with preserved remote topographical memory, in the context of a mild amnesia, also considering the extent and location of the lesion in brain areas (the right occipito-temporal region and hippocampus) involved in topographical spatial knowledge.