Sequential egocentric strategy is acquired as early as allocentric strategy: Parallel acquisition of these two navigation strategies

Igloi, Kinga; Zaoui, Mohamed; Berthoz, Alain; Rondi-Reig, Laure

doi:10.1002/hipo.20595

Cited by 130 publications

(157 citation statements)

References 30 publications

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“…Consequently, it is not necessary to encode another landmark despite shifting navigation strategy, which would explain the continued preference for attending to the route congruent landmark at test. Secondly, several studies suggest place and response learning occur in parallel (Cassel et al, 2012;Iglói et al, 2009;Marchette et al, 2011;Packard & McGaugh, 1996). In our paradigm, only one landmark supports the simultaneous acquisition of the configuration, associative cue and beacon strategies; the route congruent landmark.…”

Section: Discussionmentioning

confidence: 67%

“…In this study, participants initially employed a beacon response strategy, before shifting to a configural place strategy, replicating shifts from a response strategy to a place strategy found in previous studies (Cassel, Kelche, Lecourtier & Cassel, 2012;Iglói, Zaoui, Berthoz & Rondi-Reig, 2009). While it is not surprising that participants increasingly adopted the most successful navigation strategy over the course of the experiment, our results contrast with findings that suggest hippocampus dependent place strategies develop earlier in the learning process and are acquired faster than striatal dependent response strategies (Iaria et al, 2003;Packard & McGaugh, 1996;Schmitzer-Torbet, 2007).…”

Section: Discussionmentioning

confidence: 84%

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Human place and response learning: navigation strategy selection, pupil size and gaze behavior

Condappa

Wiener

2014

Psychological Research

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In this study, we examined the cognitive processes and ocular behavior associated with on-going navigation strategy choice using a route learning paradigm that distinguishes between three different wayfinding strategies: an allocentric place strategy, and the egocentric associative cue and beacon response strategies. Participants approached intersections of a known route from a variety of directions, and were asked to indicate the direction in which the original route continued. Their responses in a subset of these test trials allowed the assessment of strategy choice over the course of six experimental blocks. The behavioral data revealed an initial maladaptive bias for a beacon response strategy, with shifts in favour of the optimal configuration place strategy occurring over the course of the experiment. Response time analysis suggests that the configuration strategy relied on spatial transformations applied to a viewpoint-dependent spatial representation, rather than direct access to an allocentric representation. Furthermore, pupillary measures reflected the employment of place and response strategies throughout the experiment, with increasing use of the more cognitively demanding configuration strategy associated with increases in pupil dilation. During test trials in which known intersections were approached from different directions, visual attention was directed to the landmark encoded during learning as well as the intended movement direction. Interestingly, the encoded landmark did not differ between the three navigation strategies, which is discussed in the context of initial strategy choice and the parallel acquisition of place and response knowledge.

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Section: Discussionmentioning

confidence: 67%

Section: Discussionmentioning

confidence: 84%

Human place and response learning: navigation strategy selection, pupil size and gaze behavior

Condappa

Wiener

2014

Psychological Research

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“…The Starmaze task gives the possibility to assess the free choice of two spatial navigation representations: an allocentric and a sequential egocentric representation (21). The probe trials indicated that subjects use both allocentric and sequential egocentric representations throughout the task, which supports the idea of coexisting strategies supported by multiple parallel memory systems (5,21,26,(47)(48)(49). 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.…”

Section: Discussionmentioning

confidence: 99%

“…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%

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.

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252

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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“…Our "passive" task required participants to update their position using successive viewpoints and compare this with the route configurations stored in a cognitive map. It is therefore likely that participants continuously switched between allocentric and egocentric strategies, as is often done in real world navigation (25,47).…”

Section: Discussionmentioning

confidence: 99%

Neural correlates of virtual route recognition in congenital blindness

Kupers

Chebat

Madsen

et al. 2010

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

130

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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Sequential egocentric strategy is acquired as early as allocentric strategy: Parallel acquisition of these two navigation strategies

Cited by 130 publications

References 30 publications

Human place and response learning: navigation strategy selection, pupil size and gaze behavior

Human place and response learning: navigation strategy selection, pupil size and gaze behavior

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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