Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps

Iaria, Giuseppe; Chen, Jen Kai; Guariglia, Cecilia; Ptito, Alain; Petrides, Michael

doi:10.1111/j.1460-9568.2007.05371.x

Cited by 246 publications

(219 citation statements)

References 60 publications

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“…Lastly, our finding of smaller increases in the low frequency activity during recall as compared to acquisition together with more alpha activity during the latter may be explained by the use of the anterior FO electrodes. Such an assumption would be compatible with findings coming from an fMRI study (Iaria et al 2007) which revealed complementary roles of the anterior and posterior hippocampus in navigation with the former being involved in the formation of a cognitive map while the latter in using it.…”

Section: Discussionsupporting

confidence: 87%

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Clemens

Borbély

Weiss

et al. 2013

Neuroscience Research

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Hippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REM-dependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previous studies providing further indication that it is delta rather than theta that should be regarded as a human analogue of the animal RSA.NeuroscienceResearch, Volume 76, Issues 1-2, May-June 2013, Pages 67-75, DOI: 10.1016/j.neures.2013.03.004 HighlightsMesiotemporal EEG activity was assessed during a spatial task in epilepsy patients.Low frequency spectral power increased during all three navigation conditions.There was no change during task performance in the theta frequency band.Delta rather than theta should be regarded as a human analogue of animal theta. *Highlights (for review) Click here to download Highlights (for review): highlights.doc 2 AbstractHippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REMdependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previ...

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Section: Discussionsupporting

confidence: 87%

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Clemens

Borbély

Weiss

et al. 2013

Neuroscience Research

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“…Correspondingly, the pattern of activation in the training trials (bilateral hippocampus, medial prefrontal, and caudate) overlaps with both the allocentric and the sequential egocentric activations during probe trials. Activations that distinguished allocentric from sequential egocentric strategies included the bilateral parietooccipital sulcus: a region previously shown to be related to allocentric spatial processing (22,25,50), retrieval of spatial memories into imagery (24), and navigation (15,51). The reverse pattern (sequential egocentric vs. allocentric strategies) shows activations of the posterior insula, which corresponds to the human analog of the primate vestibular cortex (52) and posterior parietal operculum, which might be related to movement processing (53).…”

Section: Discussionmentioning

confidence: 99%

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.

254

184

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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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“…These studies have shown that the parahippocampus is involved in recognition of scenes, even when these are lacking any landmarks (12,(14)(15)(16)(17). The hippocampus and parahippocampus may fulfill different roles in spatial navigation.…”

Section: Discussionmentioning

confidence: 99%

“…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 visual-to-tactile sensory substitution device that converts visual information into electro-tactile pulses applied to the tongue (18, 19).…”

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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.

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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Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps

Cited by 246 publications

References 60 publications

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Increased mesiotemporal delta activity characterizes virtual navigation in humans

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

Neural correlates of virtual route recognition in congenital blindness

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