An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning

Schendan, Haline E.; Searl, Meghan; Melrose, Rebecca J.; Stern, Chantal E.

doi:10.1016/s0896-6273(03)00123-5

Cited by 562 publications

(603 citation statements)

References 76 publications

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“…As such, our results may be more closely related to findings of functional lateralization in the hippocampi of rodents (36) and birds (37). Overall, we suggest that involvement of the left human hippocampus in remembering narrative prose (30), learning novel sequences (38)(39)(40), and in supporting sequential egocentric representations in our study, could reflect a more general role in associative processing of sequential elements of an episode.…”

Section: Discussionsupporting

confidence: 82%

“…Furthermore, in agreement with a recent report (55), the time-courses of hippocampal and midbrain activation were highly correlated throughout the experiment. The left hippocampal activity during egocentric probe trials also decreased over successive trials, again consistent with reducing hippocampal involvement as sequential tasks become familiar (39) and learning reduces (22). These findings may relate to previous fMRI studies of novelty, in that left hippocampal activation is associated with sequential novelty (40) and right hippocampal activation is associated with spatial novelty (16).…”

Section: Discussionsupporting

confidence: 79%

“…The sequential egocentric representation defined in the Starmaze refers to a spatiotemporal association of different choice-points and requires a sequential organization of the information which may relate to findings that novel explicit (38)(39)(40) or implicit (39) sequence learning recruits the hippocampus. 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).…”

Section: Discussionmentioning

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.

255

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: Discussionsupporting

confidence: 82%

Section: Discussionsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

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.

255

184

View full text Add to dashboard Cite

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“…Firstly, increased post-sleep hippocampal activation was observed following a night of sleep; a finding that is of particular interest in light of recent evidence that sequence learning (Poldrack and Packard, 2003;Poldrack and Rodriguez, 2003), including explicit motor-sequence learning (Schendan et al, 2003), leads to recruitment of the hippocampal formation. Our results are consistent with this notion, and we speculate that as the output capabilities of the system increase following sleep, the hippocampal need for ordering these individual motor elements (key-presses) in a correct temporal series must concomitantly increase.…”

Section: Discussionmentioning

confidence: 96%

Sleep-dependent motor memory plasticity in the human brain

et al. 2005

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Abstract-Growing evidence indicates a role for sleep in off-line memory processing, specifically in post-training consolidation. In humans, sleep has been shown to trigger overnight learning on a motor-sequence memory task, while equivalent waking periods produce no such improvement. But while the behavioral characteristics of sleep-dependent motor learning become increasingly well characterized, the underlying neural basis remains unknown. Here we present functional magnetic resonance imaging data demonstrating a change in the representation of a motor memory after a night of sleep. Subjects trained on a motor-skill memory and 12 hours later, after either sleep or wake, were retested during functional magnetic resonance imaging. Following sleep relative to wake, regions of increased activation were expressed in the right primary motor cortex, medial prefrontal lobe, hippocampus and left cerebellum; changes that can support faster motor output and more precise mapping of key-press movements. In contrast, signal decreases were identified in parietal cortices, the left insular cortex, temporal pole and fronto-polar region, reflecting a reduced need for conscious spatial monitoring and a decreased emotional task burden. This evidence of an overnight, systems- A large body of evidence, spanning a wide range of neuroscientific disciplines, now describes evidence of sleepdependent learning in both humans and animals , already complemented by cellular and molecular models of sleep-dependent plasticity (Graves et al., 2001;Tononi and Cirelli, 2001;Benington and Frank, 2003). In particular, sleep has been implicated in the ongoing process of consolidation, following initial memory acquisition.Within the procedural memory domain, sleep in humans has been shown to trigger significant overnight learning enhancements, whereby performance is selectively improved across sleeping intervals, while equivalent waking periods confer no such performance benefit (for reviews see Walker, in press). Demonstrations of overnight, sleep-dependent learning have now been reported across both sensory (Karni et al., 1994;Gais et al., 2000; Stickgold et al., 2000a,b;Fenn et al., 2003;Atienza et al., 2004;Gaab et al., 2004) Regarding motor-sequence learning, Walker et al. (2002, 2003a,b) have shown that a night of sleep can trigger significant improvements in both performance speed and accuracy on a finger-tapping task, while equivalent periods of time awake do not result in any such learning enhancements. Furthermore, these overnight learning gains correlated with the amount of stage two non-rapid eye movement (NREM) sleep, particularly late in the night (Walker et al., 2002). Adding to these findings, it also appears that there is no transfer of sleep-dependent procedural learning to either new motor sequences, or to performance of the same sequence using the opposite hand (Fischer et al., 2002;Korman et al., 2003), suggesting that the influence of sleep is highly specific. But while the behavioral characteristics of sleep-dependent motor...

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“…The PON1 encompasses hippocampal activation that may be related to implicit and explicit memory demands under the stimulation sequence in our paradigms (Schendan et al. 2003; Henke 2010). The IC time courses shown in Figure 4 clearly exhibit olfactory task‐related behavior during visual‐only conditions supporting associative learning in olfaction.…”

Section: Discussionmentioning

confidence: 99%

Rapidly acquired multisensory association in the olfactory cortex

et al. 2015

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BackgroundThe formation of an odor percept in humans is strongly associated with visual information. However, much less is known about the roles of learning and memory in shaping the multisensory nature of odor representations in the brain.MethodThe dynamics of odor and visual association in olfaction was investigated using three functional magnetic resonance imaging (fMRI) paradigms. In two paradigms, a visual cue was paired with an odor. In the third, the same visual cue was never paired with an odor. In this experimental design, if the visual cue was not influenced by odor–visual pairing, then the blood‐oxygen‐level‐dependent (BOLD) signal elicited by subsequent visual cues should be similar across all three paradigms. Additionally, intensity, a major dimension of odor perception, was used as a modulator of associative learning which was characterized in terms of the spatiotemporal behavior of the BOLD signal in olfactory structures.ResultsA single odor–visual pairing cue could subsequently induce primary olfactory cortex activity when only the visual cue was presented. This activity was intensity dependent and was also detected in secondary olfactory structures and hippocampus.ConclusionThis study provides evidence for a rapid learning response in the olfactory system by a visual cue following odor and visual cue pairing. The novel data and paradigms suggest new avenues to explore the dynamics of odor learning and multisensory representations that contribute to the construction of a unified odor percept in the human brain.

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An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning

Cited by 562 publications

References 76 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

Sleep-dependent motor memory plasticity in the human brain

Rapidly acquired multisensory association in the olfactory cortex

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