Increased mesiotemporal delta activity characterizes virtual navigation in humans

Abstract

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...

Multifaceted roles for low-frequency oscillations in bottom-up and top-down processing during navigation and memory

“…This in turn could explain why oscillatory frequency may show an inverse relationship with brain size across species (Robinson, 1980, Herculano-Houzel, 2009). We note, though, that both non-invasive and semi-invasive recording approaches have also identified oscillations in the delta-theta band emanating from the MTL (de Araujo et al, 2002, Cornwell et al, 2008, Cornwell et al, 2012, Kaplan et al, 2012, Clemens et al, 2013). If greater number of phase cancelling sources alone is responsible for the difference in low-frequency oscillations between rats and primates, the presence of oscillations as far away as the scalp seems to weigh against this argument.…”

“…Because MEG source localization to areas such as the MTL likely has an accuracy on the order of centimeters (Barnes et al, 2004), these methods cannot unambiguously pinpoint activity to specific sub-areas of the MTL. Human semi-invasive recordings that involve placing electrodes via entrance through the foramen ovale also suggest the presence of low-frequency movement-related oscillations emanating from the MTL during VR navigation (Clemens et al, 2013). A non-human primate study also demonstrated theta oscillations and spike/phase coupling in the MTL (entorhinal cortex) when monkeys looked at objects (Killian et al, 2012), which the authors related to movement-related changes.…”

Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory

“…B 369: 20130304 behaviours (figure 3b). Oscillations at 1-4 Hz most often increased in amplitude during periods of virtual movement compared with stillness ( [54], see also [57]). Follow-up work showed that, such as theta in rodents [30], the amplitude of these 1-4 Hz oscillations positively correlated with the speed of movement [55].…”

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

“…Indeed, growing evidence indicates that slow theta activity (peaking at 3 Hz) in the human hippocampus may be the functional equivalent to the hippocampal theta rhythm of rodents (Jacobs, 2014;Watrous et al, 2013). 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).…”