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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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Temporal attenuation of amygdala object novelty effect. Above: Left amygdala activity (peak: x = −27; y = −1; z = −14; Z-score = 3.65) corresponding object novelty (novel versus familiar objects) showed a linear decrease over the course of the learning phase as relative novelty decreased. Below: Percent signal change extracted from a 10 mm sphere around the peak left amygdala voxel averaged across 18 participants for novel versus familiar objects for the first to fourth quartile of the learning phase. Activations are shown at the uncorrected threshold of P < 0.001 and overlaid on the Montreal Neurological Institute 152 T1 image for display purposes. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
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fig03: Temporal attenuation of amygdala object novelty effect. Above: Left amygdala activity (peak: x = −27; y = −1; z = −14; Z-score = 3.65) corresponding object novelty (novel versus familiar objects) showed a linear decrease over the course of the learning phase as relative novelty decreased. Below: Percent signal change extracted from a 10 mm sphere around the peak left amygdala voxel averaged across 18 participants for novel versus familiar objects for the first to fourth quartile of the learning phase. Activations are shown at the uncorrected threshold of P < 0.001 and overlaid on the Montreal Neurological Institute 152 T1 image for display purposes. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Mentions: We investigated how the above environmental and object novelty effects changed across time during the learning phase. We split learning phases into four quartiles (matching the four repetitions of object-location encoding during the learning phase) and assessed both environmental and object novelty across these quartiles. Searching for a linear decrease of environmental novelty from quartiles 1–4 failed to reveal any significant regions in the MTL or neocortex. However, a significant linear decrease in the object novelty effect (i.e., novel – familiar) from the first to fourth quartile was seen in the left amygdala (peak: x = −27; y = −1; z = −14; Z-score = 3.65; uncorrected P = 0.000131; FWE SVC P =.074), left lateral occipital cortex (peak: x = −30; y = −85; z = −20; Z-score = 4.50), left fusiform gyrus (peak: x = −48; y = −55; z = −17; Z-score = 3.74), and left posterior parahippocampal cortex (peak: x = −36; y = −37; z = −17; Z-score = 3.87). See Figure 3. Other areas showing a significant decrease in the object novelty effect from the first to fourth quartile were the bilateral ventrolateral prefrontal cortex, ventromedial prefrontal cortex, left middle temporal gyrus, and right angular gyrus. These analyses add to our original object novelty effects (comparing whole sessions) by revealing several novelty signals that attenuate within each session. By contrast, environmental novelty signals appear to attenuate only over the slower timescale of sessions, perhaps indicating that learning environmental layout is a slower process than some of the short-term effects of object novelty.


Human hippocampal processing of environmental novelty during spatial navigation.

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

Temporal attenuation of amygdala object novelty effect. Above: Left amygdala activity (peak: x = −27; y = −1; z = −14; Z-score = 3.65) corresponding object novelty (novel versus familiar objects) showed a linear decrease over the course of the learning phase as relative novelty decreased. Below: Percent signal change extracted from a 10 mm sphere around the peak left amygdala voxel averaged across 18 participants for novel versus familiar objects for the first to fourth quartile of the learning phase. Activations are shown at the uncorrected threshold of P < 0.001 and overlaid on the Montreal Neurological Institute 152 T1 image for display purposes. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig03: Temporal attenuation of amygdala object novelty effect. Above: Left amygdala activity (peak: x = −27; y = −1; z = −14; Z-score = 3.65) corresponding object novelty (novel versus familiar objects) showed a linear decrease over the course of the learning phase as relative novelty decreased. Below: Percent signal change extracted from a 10 mm sphere around the peak left amygdala voxel averaged across 18 participants for novel versus familiar objects for the first to fourth quartile of the learning phase. Activations are shown at the uncorrected threshold of P < 0.001 and overlaid on the Montreal Neurological Institute 152 T1 image for display purposes. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
Mentions: We investigated how the above environmental and object novelty effects changed across time during the learning phase. We split learning phases into four quartiles (matching the four repetitions of object-location encoding during the learning phase) and assessed both environmental and object novelty across these quartiles. Searching for a linear decrease of environmental novelty from quartiles 1–4 failed to reveal any significant regions in the MTL or neocortex. However, a significant linear decrease in the object novelty effect (i.e., novel – familiar) from the first to fourth quartile was seen in the left amygdala (peak: x = −27; y = −1; z = −14; Z-score = 3.65; uncorrected P = 0.000131; FWE SVC P =.074), left lateral occipital cortex (peak: x = −30; y = −85; z = −20; Z-score = 4.50), left fusiform gyrus (peak: x = −48; y = −55; z = −17; Z-score = 3.74), and left posterior parahippocampal cortex (peak: x = −36; y = −37; z = −17; Z-score = 3.87). See Figure 3. Other areas showing a significant decrease in the object novelty effect from the first to fourth quartile were the bilateral ventrolateral prefrontal cortex, ventromedial prefrontal cortex, left middle temporal gyrus, and right angular gyrus. These analyses add to our original object novelty effects (comparing whole sessions) by revealing several novelty signals that attenuate within each session. By contrast, environmental novelty signals appear to attenuate only over the slower timescale of sessions, perhaps indicating that learning environmental layout is a slower process than some of the short-term effects of object novelty.

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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