Human Hippocampal and Parahippocampal Theta during Goal-Directed Spatial Navigation Predicts Performance on a Virtual Morris Water Maze

Cornwell, Brian R.; Johnson, Linda L.; Holroyd, Tom; Carver, Frederick W.; Grillon, Christian

doi:10.1523/jneurosci.5001-07.2008

Cited by 205 publications

(242 citation statements)

References 51 publications

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“…This is consistent with other MEG experiments evaluating memory and spatial navigation which have also reported hippocampal effects at slower theta frequencies (Cornwell et al, 2008;Kaplan et al, 2012;Staudigl and Hanslmayr, 2013). Although it has been suggested that the hippocampus may form a closed electric field due to its sym metrical morphology (Lorente de No, 1947), this would require that the entire structure be simultaneously activated, a rather unlikely sce nario under typical experimental conditions.…”

Section: Successful Reconstruction Of Slow Theta Sources In the Hipposupporting

confidence: 90%

“…Here, we investigated the relationship between hippocampal slow theta activity and subsequent spatial memory accuracy in navigation. Although previous MEG studies evaluating subsequent navigation performance seem to support this hypothesis (Cornwell et al, 2008;Kaplan et al, 2012), slow theta activity related to the forma tion of item location associations during navigation has not been directly assessed until now. To make this possible, we administered the navigation task in the form of a subsequent memory paradigm where pictures of buildings were presented at particular spatial loca tions in a virtual grass field.…”

Section: Discussionmentioning

confidence: 98%

“…For example, when previous findings in rats (Vanderwolf, 1969) were replicated in neurosurgical patients with depth recordings in hip pocampus, it was observed that activity in slower frequencies (1 4 Hz) increased with movement in virtual navigation (Clemens et al, 2013;Ekstrom et al, 2005;Watrous et al, 2011). In addition, MEG studies have shown that better navigation performance is related to increased hippocampal activity at slow theta frequencies (Cornwell et al, 2008;Kaplan et al, 2012).…”

Section: Introductionmentioning

confidence: 93%

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Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

et al. 2016

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a b s t r a c tHuman hippocampal theta oscillations play a key role in accurate spatial coding. Associative encoding involves similar hippocampal networks but, paradoxically, is also characterized by theta power decreases. Here, we inves tigated how theta activity relates to associative encoding of place contexts resulting in accurate navigation. Using MEG, we found that slow theta (2 5 Hz) power negatively correlated with subsequent spatial accuracy for vir tual contextual locations in posterior hippocampus and other cortical structures involved in spatial cognition. A rare opportunity to simultaneously record MEG and intracranial EEG in an epilepsy patient provided crucial in sights: during power decreases, slow theta in right anterior hippocampus and left inferior frontal gyrus phase led the left temporal cortex and predicted spatial accuracy. Our findings indicate that decreased slow theta activ ity reflects local and long range neural mechanisms that encode accurate spatial contexts, and strengthens the view that local suppression of low frequency activity is essential for more efficient processing of detailed information.

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Section: Successful Reconstruction Of Slow Theta Sources In the Hipposupporting

confidence: 90%

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 93%

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Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

et al. 2016

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“…These report reconstructed sources of theta within hippocampal (or parahippocampal) structures during task performance (Tesche & Karhu, 2000;Cornwell et al, 2008). Given that source reconstruction models suffer from important limitations in detecting sources in deep brain structures with a close geometry (Alarcon et al 1994;Wiederin et al 1999) these results are unconvincing.…”

Section: Discussionmentioning

confidence: 99%

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Clemens

Borbély

Weiss

et al. 2013

Neuroscience Research

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Hippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REM-dependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previous studies providing further indication that it is delta rather than theta that should be regarded as a human analogue of the animal RSA.NeuroscienceResearch, Volume 76, Issues 1-2, May-June 2013, Pages 67-75, DOI: 10.1016/j.neures.2013.03.004 HighlightsMesiotemporal EEG activity was assessed during a spatial task in epilepsy patients.Low frequency spectral power increased during all three navigation conditions.There was no change during task performance in the theta frequency band.Delta rather than theta should be regarded as a human analogue of animal theta. *Highlights (for review) Click here to download Highlights (for review): highlights.doc 2 AbstractHippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REMdependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previ...

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“…The hippocampus and parahippocampal cortices exhibit theta oscillations during spatial navigation in rodents that are thought to mediate spatial memory formation. Neuromagnetic activity was recorded with a wholehead 275-channel magnetoencephalographic system as healthy participants navigated to a hidden platform in a virtual reality Morris water maze [91]. Analysis revealed greater theta activity in the left anterior hippocampus and parahippocampal cortices during goal-directed navigation relative to aimless movements in a sensorimotor control condition.…”

Section: Comparing Memory Island To Traditional Spatial Tests Of Humamentioning

confidence: 99%

Neuroscience-based Tests for Assessing Cognitive Changes in Normal Aging and in the Prodromal Phase of Alzheimer’s Disease

Woodruff-Pak

Raber

2012

Curr Transl Geriatr Exp Gerontol Rep

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Slow decline in cognition is key to the clinical diagnosis of Alzheimer's disease (AD). This diagnosis relies on screening tests insensitive to detection of prodromal AD, which occurs years before the appearance of clinical symptoms. Neuroscience-based tests of eyeblink classical conditioning, spatial navigation, and object recognition are associated with synaptic-level function. They show promise in detecting early changes in AD-impacted memory circuits. Eyeblink conditioning engages synapses dependent upon nicotinic acetylcholine receptors and medial septal cholinergic input to the hippocampus. Spatial navigation and object recognition engage perforant pathway entorhinal cortical input to the hippocampus. Synapses in these circuits are among the earliest impacted by beta amyloid. These three translational tests are well characterized in normal aging and AD in humans and pertinent animal models, including organisms expressing the AD risk factor apolipoprotein E4. They may detect cognitive decline in prodromal AD and prove useful for population screening and evaluation of therapeutic interventions.

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Human Hippocampal and Parahippocampal Theta during Goal-Directed Spatial Navigation Predicts Performance on a Virtual Morris Water Maze

Cited by 205 publications

References 51 publications

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Neuroscience-based Tests for Assessing Cognitive Changes in Normal Aging and in the Prodromal Phase of Alzheimer’s Disease

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