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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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Experimental Structure. A: Experimental environments shown from the participants' (first-person) perspective. Four different environments are presented in eight experimental sessions. The first two sessions (always the desert environments) provided practice outside of the scanner. Sessions 3–8 contained three novel-familiar environment repetitions with environment order, counterbalanced across participants. B: Learning phase trial structure. During learning trials, participants use a button box to navigate and “collect” three novel and three familiar (previously presented) objects (vase shown as example) four times each (a total of 24 trials per session). C: The object replacement phase, trial structure. After being cued for 3 s with a picture of an object that had been collected in the learning phase of the current session, participants were placed back in the environment and had to navigate to where they thought the object (object replacement) had been located during that learning period. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
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fig01: Experimental Structure. A: Experimental environments shown from the participants' (first-person) perspective. Four different environments are presented in eight experimental sessions. The first two sessions (always the desert environments) provided practice outside of the scanner. Sessions 3–8 contained three novel-familiar environment repetitions with environment order, counterbalanced across participants. B: Learning phase trial structure. During learning trials, participants use a button box to navigate and “collect” three novel and three familiar (previously presented) objects (vase shown as example) four times each (a total of 24 trials per session). C: The object replacement phase, trial structure. After being cued for 3 s with a picture of an object that had been collected in the learning phase of the current session, participants were placed back in the environment and had to navigate to where they thought the object (object replacement) had been located during that learning period. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Mentions: We examined the effects of environmental and object novelty on fMRI activity during a virtual spatial memory paradigm, similar to tasks used with rodents (see also Doeller et al. 2008, 2010; Kaplan et al., 2012), see Figure 1. Participants used a button box to navigate a first person perspective within virtual environments. Within each session, they learned the locations of six objects encountered within the environment, over four trials per object. In the replacement phase of the experiment, they were then cued by a picture of an object, replaced in the environment and had to navigate to the object's location, for one trial per object. Each session in a novel environment was followed by a session in the same (now familiar) environment. Three of the objects encountered in a session were new to that session and three had been encountered before in a different environment (see Fig. 1).


Human hippocampal processing of environmental novelty during spatial navigation.

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

Experimental Structure. A: Experimental environments shown from the participants' (first-person) perspective. Four different environments are presented in eight experimental sessions. The first two sessions (always the desert environments) provided practice outside of the scanner. Sessions 3–8 contained three novel-familiar environment repetitions with environment order, counterbalanced across participants. B: Learning phase trial structure. During learning trials, participants use a button box to navigate and “collect” three novel and three familiar (previously presented) objects (vase shown as example) four times each (a total of 24 trials per session). C: The object replacement phase, trial structure. After being cued for 3 s with a picture of an object that had been collected in the learning phase of the current session, participants were placed back in the environment and had to navigate to where they thought the object (object replacement) had been located during that learning period. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4255751&req=5

fig01: Experimental Structure. A: Experimental environments shown from the participants' (first-person) perspective. Four different environments are presented in eight experimental sessions. The first two sessions (always the desert environments) provided practice outside of the scanner. Sessions 3–8 contained three novel-familiar environment repetitions with environment order, counterbalanced across participants. B: Learning phase trial structure. During learning trials, participants use a button box to navigate and “collect” three novel and three familiar (previously presented) objects (vase shown as example) four times each (a total of 24 trials per session). C: The object replacement phase, trial structure. After being cued for 3 s with a picture of an object that had been collected in the learning phase of the current session, participants were placed back in the environment and had to navigate to where they thought the object (object replacement) had been located during that learning period. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
Mentions: We examined the effects of environmental and object novelty on fMRI activity during a virtual spatial memory paradigm, similar to tasks used with rodents (see also Doeller et al. 2008, 2010; Kaplan et al., 2012), see Figure 1. Participants used a button box to navigate a first person perspective within virtual environments. Within each session, they learned the locations of six objects encountered within the environment, over four trials per object. In the replacement phase of the experiment, they were then cued by a picture of an object, replaced in the environment and had to navigate to the object's location, for one trial per object. Each session in a novel environment was followed by a session in the same (now familiar) environment. Three of the objects encountered in a session were new to that session and three had been encountered before in a different environment (see Fig. 1).

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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