Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans

Baumann, Oliver; Chan, Edgar; Mattingley, Jason B.

doi:10.1016/j.neuroimage.2009.10.021

Cited by 84 publications

(87 citation statements)

References 58 publications

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“…Our observation of enhanced activity in the parahippocampal gyri when participants viewed static snapshots from the negatively conditioned room might reflect strengthened representations of learned place information. In a previous study, we found that increased parahippocampal activity during encoding was predictive of more accurate memory-based navigation in the absence of affective events (Baumann et al, 2010). Neuropsychological data further emphasize the importance of the parahippocampal cortex in navigational processes.…”

Section: Discussionsupporting

confidence: 49%

“…The parahippocampal cortex forms part of a network of medial-temporal and parietal regions that is thought to be involved in different types of spatial processing (Mullally & Maguire, 2011;Baumann et al, 2010;Ohnishi, Matsuda, Hirakata, & Ugawa, 2006;Ploner et al, 2000;Bohbot et al, 1998;Maguire et al, 1998). Its main function has been attributed to perceptual encoding and retrieval of place and scene information (Epstein, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…Extensive research has attributed the encoding and recall of place and scene information during navigation to the parahippocampal cortex (Baumann, Chan, & Mattingley, 2010;Epstein, 2008;Maguire, Frith, Burgess, Donnett, & OʼKeefe, 1998). Moreover, recent studies have suggested that the parahippocampal cortex automatically codes for the navigational relevance of objects in the environment (e.g., Janzen, Wagensveld, & van Turennout, 2007;Janzen & van Turennout, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Negative Emotional Experiences during Navigation Enhance Parahippocampal Activity during Recall of Place Information

Chan

Baumann

Bellgrove

et al. 2014

Journal of Cognitive Neuroscience

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Abstract■ It is known that the parahippocampal cortex is involved in object-place associations in spatial learning, but it remains unknown whether activity within this region is modulated by affective signals during navigation. Here we used fMRI to measure the neural consequences of emotional experiences on place memory during navigation. A day before scanning, participants undertook an active object location memory task within a virtual house in which each room was associated with a different schedule of task-irrelevant emotional events. The events varied in valence (positive, negative, or neutral) and in their rate of occurrence (intermittent vs. constant). On a subsequent day, we measured neural activity while participants were shown static images of the previously learned virtual environment, now in the absence of any affective stimuli. Our results showed that parahippocampal activity was significantly enhanced bilaterally when participants viewed images of a room in which they had previously encountered negatively arousing events. We conclude that such automatic enhancement of place representations by aversive emotional events serves as an important adaptive mechanism for avoiding future threats. ■

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Section: Discussionsupporting

confidence: 49%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Negative Emotional Experiences during Navigation Enhance Parahippocampal Activity during Recall of Place Information

Chan

Baumann

Bellgrove

et al. 2014

Journal of Cognitive Neuroscience

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“…This analysis revealed a small region of increased activity in the novel versus repeated condition that was restricted to the dorsal striatum bilaterally (MNI coordinates of the peak voxel: 24, 12, 2 and Ϫ20, 0, 4). This region has been implicated previously in the retrieval of spatial information during active navigation (Iaria et al, 2003;Doeller et al, 2008;Baumann et al, 2010) but to date has not been associated explicitly with perceived heading.…”

Section: Test Phasementioning

confidence: 98%

Medial Parietal Cortex Encodes Perceived Heading Direction in Humans

Baumann¹,

Mattingley²

2010

J. Neurosci.

127

114

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The ability to encode and update representations of heading direction is crucial for successful navigation. In rats, head-direction cells located within the limbic system alter their firing rate in accordance with the animal's current heading. To date, however, the neural structures that underlie an allocentric or viewpoint-independent sense of direction in humans remain unknown. Here we used functional magnetic resonance imaging (fMRI) to measure neural adaptation to distinctive landmarks associated with one of four heading directions in a virtual environment. Our experiment consisted of two phases: a "learning phase," in which participants actively navigated the virtual maze; and a "test phase," in which participants viewed pairs of images from the maze while undergoing fMRI. We found that activity within the medial parietal cortex-specifically, Brodmann area 31-was modulated by learned heading, suggesting that this region contains neural populations involved in the encoding and retrieval of allocentric heading information in humans. These results are consistent with clinical case reports of patients with acquired lesions of medial posterior brain regions, who exhibit deficits in forming and recalling links between landmarks and directional information. Our findings also help to explain why navigation disturbances are commonly observed in patients with Alzheimer's disease, whose pathology typically includes the cortical region we have identified as being crucial for maintaining representations of heading direction.

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“…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). Possibly related to a role in landmarkbased encoding, objects in isolation activate the PHG according to their associated spatial context.…”

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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Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans

Cited by 84 publications

References 58 publications

Negative Emotional Experiences during Navigation Enhance Parahippocampal Activity during Recall of Place Information

Negative Emotional Experiences during Navigation Enhance Parahippocampal Activity during Recall of Place Information

Medial Parietal Cortex Encodes Perceived Heading Direction in Humans

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

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