Mental navigation along memorized routes activates the hippocampus, precuneus, and insula

Ghaëm, O.; Mellet, Emmanuel; Crivello, Fabrice; Tzourio, N.; Mazoyer, Bernard; Berthoz, CA Alain; Denis, Michel

doi:10.1097/00001756-199702100-00032

Cited by 406 publications

(301 citation statements)

References 16 publications

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“…In our study, blind but not blindfolded sighted participants activated the right posterior parahippocampus during route recognition. This is in line with the results of brain imaging studies in sighted subjects during spatial navigation under full vision in virtual environments (9,11,12,24,27), during mental navigation of an old, known environment (28)(29)(30)(31), and during visual scene processing (14,15). We here show that the same area is activated in congenitally blind subjects when spatial information is provided through the tactile modality.…”

Section: Discussionsupporting

confidence: 91%

Neural correlates of virtual route recognition in congenital blindness

Kupers

Chebat

Madsen

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

127

133

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Despite the importance of vision for spatial navigation, blind subjects retain the ability to represent spatial information and to move independently in space to localize and reach targets. However, the neural correlates of navigation in subjects lacking vision remain elusive. We therefore used functional MRI (fMRI) to explore the cortical network underlying successful navigation in blind subjects. We first trained congenitally blind and blindfolded sighted control subjects to perform a virtual navigation task with the tongue display unit (TDU), a tactile-to-vision sensory substitution device that translates a visual image into electrotactile stimulation applied to the tongue. After training, participants repeated the navigation task during fMRI. Although both groups successfully learned to use the TDU in the virtual navigation task, the brain activation patterns showed substantial differences. Blind but not blindfolded sighted control subjects activated the parahippocampus and visual cortex during navigation, areas that are recruited during topographical learning and spatial representation in sighted subjects. When the navigation task was performed under full vision in a second group of sighted participants, the activation pattern strongly resembled the one obtained in the blind when using the TDU. This suggests that in the absence of vision, cross-modal plasticity permits the recruitment of the same cortical network used for spatial navigation tasks in sighted subjects.cross-modal plasticity | parahippocampus | sensory substitution | spatial navigation | visual cortex T he ability to navigate efficiently in large-scale environments was always a predicate for human survival, now applied to the particular challenges of living in a modern, urban society. Visual cues signaling the location of landmarks play a key role in facilitating the formation of spatial cognitive maps used for path finding in a visual setting (1, 2). Despite the importance of vision in spatial cognition, the abilities to recognize a traveled route and to represent spatial information are maintained in blind individuals (3-5), probably through tactile, auditory, and olfactory cues, as well as motion-related cues arising from the vestibular and proprioceptive systems.During successful navigation, spatial information needs to be encoded and retrieved. The role of the hippocampus for navigation in large-scale environments has been amply demonstrated in both animal (6-8) and human studies (9-11). Besides the hippocampus, several other areas in the posterior mesial lobe and posterior parietal, occipital, and infero-temporal cortices also play an important role in navigation (9,(12)(13)(14)(15)(16)(17).The neural correlates of navigation in congenital blindness remain elusive, in part owing to the difficulty in testing navigational skills of blind subjects within the setting of a functional brain imaging study. To circumvent this difficulty, we trained blind and sighted subjects in a spatial navigation task using the tongue display unit (TDU), a vis...

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Section: Discussionsupporting

confidence: 91%

Neural correlates of virtual route recognition in congenital blindness

Kupers

Chebat

Madsen

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

127

133

View full text Add to dashboard Cite

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“…Left-lateralized hippocampal activation for sequential egocentric representations also supports the idea that the left hippocampus mediates spatiotemporal associations between the multiple events that constitute the elements of an episodic memory (2, 41). This finding is consistent with hippocampal involvement in sequential route-based navigation in rodents (14) and the planning of complex routes in human (15,42).…”

Section: Discussionsupporting

confidence: 83%

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

Igloi

Doeller

Berthoz

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

247

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The hippocampus is crucial for both spatial navigation and episodic memory, suggesting that it provides a common function to both. Here we adapt a spatial paradigm, developed for rodents, for use with functional MRI in humans to show that activation of the right hippocampus predicts the use of an allocentric spatial representation, and activation of the left hippocampus predicts the use of a sequential egocentric representation. Both representations can be identified in hippocampal activity before their effect on behavior at subsequent choice-points. Our results suggest that, rather than providing a single common function, the two hippocampi provide complementary representations for navigation, concerning places on the right and temporal sequences on the left, both of which likely contribute to different aspects of episodic memory.T he hippocampus plays a crucial role in both spatial navigation and episodic memory (1-6). However, the nature of the fundamental hippocampal process or representation that might underlie both functions remains the subject of intense speculation, including suggestions that it is best characterized as associative (7), sequential (8), flexible relational (2), allocentric (1, 5, 9), or spatial contextual (4, 5). Similar speculation surrounds the nature of any lateralization of these representations (1, 5, 10), and whether the firing of hippocampal neurons in freely moving rodents reflects allocentric position, spatial context, or sequential position along a route (5, 11, 12). Here we show that the hippocampus predicts and supports navigation via sequential representations in the left hippocampus and allocentric spatial representations in the right hippocampus. These complementary lateralized representations suggest an explanation for the multiple hippocampal contributions to different aspects of spatial and episodic memory.Within spatial memory a distinction has been made between "allocentric" (world-centered) and "egocentric" (body-centered) representations, with allocentric (or place-learning) and simple egocentric (stimulus response-like) navigation shown to depend on the hippocampus and dorsal striatum, respectively, in rodents (5, 13). recently demonstrated that an additional sequential egocentric representation depends on the rodent hippocampus. The human hippocampus has likewise been associated with allocentric representations of location, allowing accurate navigation from new starting locations (15) based on the configuration of environmental cues (16, 17) or recognition of locations from a new viewpoint (18,19). Similarly, navigation via a fixed route (15, 17) or relative to a single landmark (16), consistent with simple egocentric representations, has been associated with the dorsal striatum. However, to our knowledge, the neural bases of the sequential egocentric representation have not yet been identified in humans, and could provide a link between spatial navigation and episodic memory.Here we adapt the Starmaze task developed for mice (14,20) to investigate the neural base...

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“…For example, tasks requiring memory of routes learned from the environment (Ghaem et al, 1997;Mellet et al, 2000) activate RSC and lesions, strokes, or tumors in this region produce amnesia including topokinetic disorientation (Valenstein et al, 1987;Rudge and Warrington, 1991;Takahashi et al, 1997). In view of the direct connections between RSC and dPCC and participation in common functions, the bCCOI analysis showed a restricted cingulate gyrus pattern of correlated voxels most prominently located in the posterior MCC and PCC, although there was an additional extension along the rostrum of the corpus callosum.…”

Section: Retrosplenial Cortexmentioning

confidence: 99%

“…Strokes in right hemisphere RSC/PCC can produce topographic disorientation (Takahashi et al, 1997) as did a splenial glioma (Bottini et al, 1990), while those in the left hemisphere and tumors pressing preferentially on the left RSC produced severe anterograde and retrograde memory impairments including that for verbal and visual information (Valenstein et al, 1987;Rudge and Warrington, 1991). Functional imaging has shown this region is part of a network that mediates topokinetic (spatial) navigation and memory (Ghaem et al, 1997;Maguire et al, 1997;Berthoz, 1997Berthoz, , 1999. Alert monkey studies by Olson et al (1993Olson et al ( , 1996 showed that neurons in the dorsal PCC were active while assessing large visual field patterns and activity was tightly linked to the position of the eye in the orbit and the direction and amplitude of saccadic eye movements.…”

Section: Introductionmentioning

confidence: 99%

Cytology and functionally correlated circuits of human posterior cingulate areas

2006

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Human posterior cingulate cortex (PCC) and retrosplenial cortex (RSC) form the posterior cingulate gyrus, however, monkey connection and human imaging studies suggest that PCC area 23 is not uniform and atlases mislocate RSC. We histologically assessed these regions in 6 postmortem cases, plotted a flat map, and characterized differences in dorsal (d) and ventral (v) area 23. Subsequently, functional connectivity of histologically guided regions of interest (ROI) were assessed in 163 [ 18 F] fluorodeoxyglucose human cases with PET. Compared to area d23, area v23 had a higher density and larger pyramids in layers II, IIIc, and Vb and more intermediate neurofilament-expressing neurons in layer Va. Coregisrtration of each case to standard coordinates showed that the ventral branch of the splenial sulci coincided with the border between d/v PCC at −5.4±0.17 cm from the vertical plane and +1.97±0.08 cm from the bi-commissural line. Correlation analysis of glucose metabolism using histologically guided ROIs suggested important circuit differences including dorsal and ventral visual stream inputs, interactions between the vPCC and subgenual cingulate cortex, and preferential relations between dPCC and the cingulate motor region. The RSC, in contrast, had restricted correlated activity with pericallosal cortex and thalamus. Visual information may be processed with an orbitofrontal link for synthesis of signals to drive premotor activity through dPCC. Review of the literature in terms of a PCC duality suggests that interactions of dPCC, including area 23d, orients the body in space via the cingulate motor areas, while vPCC interacts with subgenual cortex to process self-relevant emotional and non-emotional information and objects and self reflection.

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Mental navigation along memorized routes activates the hippocampus, precuneus, and insula

Cited by 406 publications

References 16 publications

Neural correlates of virtual route recognition in congenital blindness

Neural correlates of virtual route recognition in congenital blindness

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

Cytology and functionally correlated circuits of human posterior cingulate areas

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