The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze

Weniger, Godehard; Siemerkus, Jakob; Schmidt‐Samoa, Carsten; Mehlitz, Markus; Baudewig, Jürgen; Dechent, Peter; Irle, Eva

doi:10.1016/j.nlm.2009.08.003

Cited by 54 publications

(48 citation statements)

References 62 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%

“…The hippocampus and parahippocampus may fulfill different roles in spatial navigation. For instance, a recent fMRI study showed that the parahippocampus is involved in egocentric spatial learning (24), whereas the hippocampus may be more involved in allocentric spatial representations (11,25,26). In our study, blind but not blindfolded sighted participants activated the right posterior parahippocampus during route recognition.…”

Section: Discussionsupporting

confidence: 41%

“…The precuneus, posterior parietal cortex, and fusiform gyrus also play an important role in spatial cognition (9,12,13,24,(28)(29)(30)(31). Activation of the ventrolateral occipitotemporal cortex, including the parahippocampus, was reported in sighted subjects during landmark-centered judgment about object location, whereas superior parietal lobule, cuneus, precuneus, and superior and middle occipital gyri were activated by both allocentric and egocentric spatial tasks (12).…”

Section: Discussionmentioning

confidence: 99%

“…In contrast with egocentric frameworks, the location of objects within allocentric frameworks does not change when the subject moves in the environment (25). Results from brain imaging studies and studies in patients with brain lesions have suggested that the hippocampus supports allocentric processing, whereas the posterior parietal cortex and the precuneus are more involved in egocentric spatial representations (12,14,24,25).…”

Section: Discussionmentioning

confidence: 99%

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Neural correlates of virtual route recognition in congenital blindness

Kupers

Chebat

Madsen

et al. 2010

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

134

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%

Section: Discussionsupporting

confidence: 41%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Neural correlates of virtual route recognition in congenital blindness

Kupers

Chebat

Madsen

et al. 2010

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

134

133

View full text Add to dashboard Cite

show abstract

“…Imaging studies using virtual environments explored by participants from a first-person perspective showed that the encoding of topographical spatial knowledge invoked the hippocampus (Doeller, King, & Burgess, 2008;Shelton & Gabrieli, 2002;Maguire, Frackowiak, & Frith, 1996) and the parahippocampal gyrus (PHG; Weniger et al, 2010). This latter region, which shows sensitivity to the presentation of visual scenes (Epstein, 2008;Epstein & Kanwisher, 1998), is also involved in the successful encoding of spatial information based on landmarks (Baumann, Chan, & Mattingley, 2010;Maguire, Frith, Burgess, Donnett, & OʼKeefe, 1998).…”

Section: Introductionmentioning

confidence: 99%

Neural Encoding of Objects Relevant for Navigation and Resting State Correlations with Navigational Ability

Wegman

Janzen²

2011

Journal of Cognitive Neuroscience

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Abstract■ Objects along a route can help us to successfully navigate through our surroundings. Previous neuroimaging research has shown that the parahippocampal gyrus (PHG) distinguishes between objects that were previously encountered at navigationally relevant locations (decision points) and irrelevant locations (nondecision points) during simple object recognition. This study aimed at unraveling how this neural marking of objects relevant for navigation is established during learning and postlearning rest. Twenty-four participants were scanned using fMRI while they were viewing a route through a virtual environment. Eye movements were measured, and brain responses were time-locked to viewing each object. The PHG showed increased responses to decision point objects compared with nondecision point objects during route learning. We compared functional connectivity between the PHG and the rest of the brain in a resting state scan postlearning with such a scan prelearning. Results show that functional connectivity between the PHG and the hippocampus is positively related to participantsʼ self-reported navigational ability. On the other hand, connectivity with the caudate nucleus correlated negatively with navigational ability. These results are in line with a distinction between egocentric and allocentric spatial representations in the caudate nucleus and the hippocampus, respectively. Our results thus suggest a relation between navigational ability and a neural preference for a specific type of spatial representation. Together, these results show that the PHG is immediately involved in the encoding of navigationally relevant object information. Furthermore, they provide insight into the neural correlates of individual differences in spatial ability. ■

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Segregating cognitive functions within hippocampal formation: A quantitative meta‐analysis on spatial navigation and episodic memory

Kühn

Gallinat

2013

Human Brain Mapping

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The most important cognitive domains where hippocampal formation is crucially involved are navigation and memory. Some evidence suggests that different hippocampal subregions mediate these domains. However, a quantitative meta-analysis on neuroimaging studies of spatial navigation versus memory is lacking. By means of activation likelihood estimation (ALE), we investigate concurrence of brain regions activated during spatial navigation encoding and retrieval as well as during episodic memory encoding and retrieval tasks in humans. During encoding in spatial navigation, activity was located in more posterior regions of the hippocampal formation, whereas episodic memory encoding was located in more anterior regions. Retrieval in spatial navigation was more strongly lateralized to the right compared to episodic memory retrieval. Within studies on spatial navigation retrieval, immediate recall was located more posterior and delayed recall more anterior. Overlap between concurrence of activation in spatial navigation and episodic memory was rather limited in comparison to uniquely involved regions. This argues in favor of two distinct networks, one for spatial navigation the other for episodic memory within the hippocampal formation.

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The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze

Cited by 54 publications

References 62 publications

Neural correlates of virtual route recognition in congenital blindness

Neural correlates of virtual route recognition in congenital blindness

Neural Encoding of Objects Relevant for Navigation and Resting State Correlations with Navigational Ability

Segregating cognitive functions within hippocampal formation: A quantitative meta‐analysis on spatial navigation and episodic memory

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