Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus

Ino, Tadashi; Inoue, Yumiko; Kage, Masato; Hirose, Syuichi; Kimura, Tooru; Fukuyama, Hidenao

doi:10.1016/s0304-3940(02)00019-8

Cited by 109 publications

(82 citation statements)

References 20 publications

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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: 98%

“…We hypothesized that we would identify, before the first choice-point, areas of the hippocampal prefrontal striatal loop involved in supporting the allocentric and sequential egocentric representations. In addition, we would expect to see some changes in activation over the time-course of the experiment, including increased hippocampal involvement early in the task, when novelty and learning is maximal (16,22), and increased retrosplenial/ medial parietal regions later in the task, as a detailed internal representation of the environment is formed that can support mental imagery (9,17,(21)(22)(23)(24)(25).…”

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confidence: 99%

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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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Section: Discussionmentioning

confidence: 98%

mentioning

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

View full text Add to dashboard Cite

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“…A number of reports have speculated that pV6A is in the vicinity of the parieto-occipital sulcus; however, there has been considerable variability in the specific location. Human pV6A has been proposed to lie near the junction of the POS and calcarine sulcus (Ino et al, 2002;Dechent and Frahm, 2003;Bristow et al, 2005;Stiers et al, 2006), in the superior POS (Portin et al, 1998;Pitzalis et al, 2006a;Quinlan and Culham, 2007), and somewhat lateral to the POS (Grol et al, 2007;Verhagen et al, 2008). Localization is complicated by the fact that the fundus of the POS is only millimeters from the IPS and many studies only perform group analyses with extensive smoothing, making it difficult to pinpoint the sulcus in which the activation lies.…”

Section: Spoc In Macaques and Humansmentioning

confidence: 99%

Is That within Reach? fMRI Reveals That the Human Superior Parieto-Occipital Cortex Encodes Objects Reachable by the Hand

Gallivan¹,

Cavina-Pratesi²,

Culham³

2009

J. Neurosci.

196

173

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Macaque neurophysiology and human neuropsychology results suggest that parietal cortex encodes a unique representation of space within reach of the arm. Here, we used slow event-related functional magnetic resonance imaging (fMRI) to investigate whether human brain areas involved in reaching are more activated by objects within reach versus beyond reach. In experiment 1, graspable objects were placed at three possible locations on a platform: two reachable locations and one beyond reach. On some trials, participants reached to touch or grasp objects at the reachable location; on other trials participants passively viewed objects at one of the three locations. A reach-related area in the superior parieto-occipital cortex (SPOC) was more activated for targets within reach than beyond. In experiment 2, we investigated whether this SPOC response occurred when visual and motor confounds were controlled and whether it was modulated when a tool extended the effective range of the arm. On some trials, participants performed grasping and reaching actions to a reachable object location using either the hand alone or a tool; on other trials, participants passively viewed reachable and unreachable object locations. SPOC was significantly more active for passively viewed objects within reach of the hand versus beyond reach, regardless of whether or not a tool was available. Interestingly, these findings suggest that neural responses within brain areas coding actions (such as SPOC for reaching) may reflect automatic processing of motor affordances (such as reachability with the hand).

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“…Moreover, the retrosplenial cortex is thought to support stimulus conversion from egocentric reference frames in parietal cortex to allocentric reference frames in medial temporal regions and vice versa (Burgess et al, 2001a,b;Ino et al, 2002). Because most studies on human navigation have focused on the retrieval of previously learned environments, our goal was to identify the neural structures involved in acquiring survey knowledge from ground-level navigation.…”

Section: Introductionmentioning

confidence: 99%

Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations

Wolbers

Büchel²

2005

J. Neurosci.

291

266

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During everyday navigation, humans encounter complex environments predominantly from a first-person perspective. Behavioral evidence suggests that these perceptual experiences can be used not only to acquire route knowledge but also to directly assemble map-like survey representations. Most studies of human navigation focus on the retrieval of previously learned environments, and the neural foundations of integrating sequential views into a coherent representation are not yet fully understood. We therefore used our recently introduced virtual-reality paradigm, which provides accuracy and reaction-time measurements precisely indicating the emergence of survey knowledge, and functional magnetic resonance imaging while participants repeatedly encoded a complex environment from a first-person ground-level perspective. Before the experiment, we gave specific instructions to induce survey learning, which, based on the clear evidence for emerging survey knowledge in the behavioral data from 11 participants, proved successful. Neuroimaging data revealed increasing activation across sessions only in bilateral retrosplenial cortices, thus paralleling behavioral measures of map expertise. In contrast, hippocampal activation did not follow absolute performance but rather reflected the amount of knowledge acquired in a given session. In other words, hippocampal activation was most prominent during the initial learning phase and decayed after performance had approached ceiling level. We therefore conclude that, during navigational learning, retrosplenial areas mainly serve to integrate egocentric spatial information with cues about self-motion, whereas the hippocampus is needed to incorporate new information into an emerging memory representation.

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Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus

Cited by 109 publications

References 20 publications

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

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

Is That within Reach? fMRI Reveals That the Human Superior Parieto-Occipital Cortex Encodes Objects Reachable by the Hand

Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations

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