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Human hippocampal processing of environmental novelty during spatial navigation.

Kaplan R, Horner AJ, Bandettini PA, Doeller CF, Burgess N - Hippocampus (2014)

Bottom Line: We found greater BOLD response to novel relative to familiar environments in the hippocampus and adjacent parahippocampal gyrus.Object novelty was associated with increased activity in the posterior parahippocampal/fusiform gyrus and anterior hippocampus extending into the amygdala and superior temporal sulcus.By investigating how participants learn and use different forms of information during spatial navigation, we found that medial temporal lobe (MTL) activity reflects both the novelty of the environment and of the objects located within it.

View Article: PubMed Central - PubMed

Affiliation: NIMH-UCL Joint Graduate Partnership Program in Neuroscience, Bethesda, Maryland; UCL Institute of Cognitive Neuroscience, University College London, United Kingdom; UCL Institute of Neurology, University College London, United Kingdom; Section on Functional Imaging Methods, Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, Maryland.

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Environmental and object novelty during the navigation task. A: Left hippocampal activity corresponding to environmental novelty during navigation (above; peak voxel: x = −30; y = −28; z = −14; Z-score = 4.65; including both learning and object replacement phases). Percent signal change in a 10 mm sphere around the left hippocampal peak for all four conditions (navigating toward or replacing novel or familiar objects within novel or familiar environments, below, showing mean ± SEM over the 18 participants). B: Left anterior hippocampal activity, extending into the amygdala and superior temporal sulcus, corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 3.81). Percent signal change in a 10 mm sphere around the left anterior hippocampal peak for all four conditions (below, mean ± SEM). C: Left parahippocampal/fusiform activity corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 4.10). Percent signal change in a 10 mm sphere around the left parahippocampal/fusiform peak for all four conditions (mean ± SEM). D: Right ventral pallidum activity corresponding to the interaction between environmental novelty and experimental phase (left; peak voxel: x = 15; y = −10; z = −8; Z-score = 4.34; left ventral pallidum and midbrain/VTA effects visible in axial slice). Percent signal change in a 10 mm sphere around the right ventral pallidal peak during navigation in novel versus familiar environments during the learning and replacement phases (mean ± SEM). All activations are shown at the uncorrected threshold of P < 0.001 for display purposes and overlaid on the Montreal Neurological Institute 152 T1 image. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
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fig02: Environmental and object novelty during the navigation task. A: Left hippocampal activity corresponding to environmental novelty during navigation (above; peak voxel: x = −30; y = −28; z = −14; Z-score = 4.65; including both learning and object replacement phases). Percent signal change in a 10 mm sphere around the left hippocampal peak for all four conditions (navigating toward or replacing novel or familiar objects within novel or familiar environments, below, showing mean ± SEM over the 18 participants). B: Left anterior hippocampal activity, extending into the amygdala and superior temporal sulcus, corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 3.81). Percent signal change in a 10 mm sphere around the left anterior hippocampal peak for all four conditions (below, mean ± SEM). C: Left parahippocampal/fusiform activity corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 4.10). Percent signal change in a 10 mm sphere around the left parahippocampal/fusiform peak for all four conditions (mean ± SEM). D: Right ventral pallidum activity corresponding to the interaction between environmental novelty and experimental phase (left; peak voxel: x = 15; y = −10; z = −8; Z-score = 4.34; left ventral pallidum and midbrain/VTA effects visible in axial slice). Percent signal change in a 10 mm sphere around the right ventral pallidal peak during navigation in novel versus familiar environments during the learning and replacement phases (mean ± SEM). All activations are shown at the uncorrected threshold of P < 0.001 for display purposes and overlaid on the Montreal Neurological Institute 152 T1 image. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Mentions: We used a 2 × 2 × 2 ANOVA (Object × Environment × Phase) to test whether there were significant differences for object and environmental novelty processing during learning and object replacement phases. When contrasting navigation in novel versus familiar environments (collapsed across learning and replacement phases), the strongest increase across the whole brain was in the medial temporal lobe, with a peak in the left posterior hippocampus/parahippocampal gyrus (x = −30; y = −28; z = −14; Z-score = 4.65; SVC FWE P = 0.001; see Fig. 2A and Table3) and another subpeak that was part of the same cluster in the anterior hippocampus (x = −27; y = −19; z = −17; Z-score = 3.56).


Human hippocampal processing of environmental novelty during spatial navigation.

Kaplan R, Horner AJ, Bandettini PA, Doeller CF, Burgess N - Hippocampus (2014)

Environmental and object novelty during the navigation task. A: Left hippocampal activity corresponding to environmental novelty during navigation (above; peak voxel: x = −30; y = −28; z = −14; Z-score = 4.65; including both learning and object replacement phases). Percent signal change in a 10 mm sphere around the left hippocampal peak for all four conditions (navigating toward or replacing novel or familiar objects within novel or familiar environments, below, showing mean ± SEM over the 18 participants). B: Left anterior hippocampal activity, extending into the amygdala and superior temporal sulcus, corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 3.81). Percent signal change in a 10 mm sphere around the left anterior hippocampal peak for all four conditions (below, mean ± SEM). C: Left parahippocampal/fusiform activity corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 4.10). Percent signal change in a 10 mm sphere around the left parahippocampal/fusiform peak for all four conditions (mean ± SEM). D: Right ventral pallidum activity corresponding to the interaction between environmental novelty and experimental phase (left; peak voxel: x = 15; y = −10; z = −8; Z-score = 4.34; left ventral pallidum and midbrain/VTA effects visible in axial slice). Percent signal change in a 10 mm sphere around the right ventral pallidal peak during navigation in novel versus familiar environments during the learning and replacement phases (mean ± SEM). All activations are shown at the uncorrected threshold of P < 0.001 for display purposes and overlaid on the Montreal Neurological Institute 152 T1 image. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4255751&req=5

fig02: Environmental and object novelty during the navigation task. A: Left hippocampal activity corresponding to environmental novelty during navigation (above; peak voxel: x = −30; y = −28; z = −14; Z-score = 4.65; including both learning and object replacement phases). Percent signal change in a 10 mm sphere around the left hippocampal peak for all four conditions (navigating toward or replacing novel or familiar objects within novel or familiar environments, below, showing mean ± SEM over the 18 participants). B: Left anterior hippocampal activity, extending into the amygdala and superior temporal sulcus, corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 3.81). Percent signal change in a 10 mm sphere around the left anterior hippocampal peak for all four conditions (below, mean ± SEM). C: Left parahippocampal/fusiform activity corresponding to object novelty during navigation (above, peak voxel: x = 39; y = −40; z = −14; Z-score = 4.10). Percent signal change in a 10 mm sphere around the left parahippocampal/fusiform peak for all four conditions (mean ± SEM). D: Right ventral pallidum activity corresponding to the interaction between environmental novelty and experimental phase (left; peak voxel: x = 15; y = −10; z = −8; Z-score = 4.34; left ventral pallidum and midbrain/VTA effects visible in axial slice). Percent signal change in a 10 mm sphere around the right ventral pallidal peak during navigation in novel versus familiar environments during the learning and replacement phases (mean ± SEM). All activations are shown at the uncorrected threshold of P < 0.001 for display purposes and overlaid on the Montreal Neurological Institute 152 T1 image. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
Mentions: We used a 2 × 2 × 2 ANOVA (Object × Environment × Phase) to test whether there were significant differences for object and environmental novelty processing during learning and object replacement phases. When contrasting navigation in novel versus familiar environments (collapsed across learning and replacement phases), the strongest increase across the whole brain was in the medial temporal lobe, with a peak in the left posterior hippocampus/parahippocampal gyrus (x = −30; y = −28; z = −14; Z-score = 4.65; SVC FWE P = 0.001; see Fig. 2A and Table3) and another subpeak that was part of the same cluster in the anterior hippocampus (x = −27; y = −19; z = −17; Z-score = 3.56).

Bottom Line: We found greater BOLD response to novel relative to familiar environments in the hippocampus and adjacent parahippocampal gyrus.Object novelty was associated with increased activity in the posterior parahippocampal/fusiform gyrus and anterior hippocampus extending into the amygdala and superior temporal sulcus.By investigating how participants learn and use different forms of information during spatial navigation, we found that medial temporal lobe (MTL) activity reflects both the novelty of the environment and of the objects located within it.

View Article: PubMed Central - PubMed

Affiliation: NIMH-UCL Joint Graduate Partnership Program in Neuroscience, Bethesda, Maryland; UCL Institute of Cognitive Neuroscience, University College London, United Kingdom; UCL Institute of Neurology, University College London, United Kingdom; Section on Functional Imaging Methods, Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, Maryland.

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Related in: MedlinePlus