The functional role of human right hippocampal/parahippocampal theta rhythm in environmental encoding during virtual spatial navigation

Abstract

Low frequency theta band oscillations (4-8 Hz) are thought to provide a timing mechanism for hippocampal place cell firing and to mediate the formation of spatial memory. In rodents, hippocampal theta has been shown to play an important role in encoding a new environment during spatial navigation, but a similar functional role of hippocampal theta in humans has not been firmly established. To investigate this question, we recorded healthy participants' brain responses with a 160-channel whole-head MEG system as they performed two training sets of a virtual Morris water maze task. Environment layouts (except for platform locations) of the two sets were kept constant to measure theta activity during spatial learning in new and familiar environments. In line with previous findings, left hippocampal/parahippocampal theta showed more activation navigating to a hidden platform relative to random swimming. Consistent with our hypothesis, right hippocampal/parahippocampal theta was stronger during the first training set compared to the second one. Notably, theta in this region during the first training set correlated with spatial navigation performance across individuals in both training sets. These results strongly argue for the functional importance of right hippocampal theta in initial encoding of configural properties of an environment during spatial navigation. Our findings provide important evidence that right hippocampal/parahippocampal theta activity is associated with environmental encoding in the human brain. Hum Brain Mapp 38:1347-1361, 2017. © 2016 Wiley Periodicals, Inc.

Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans

“…One might reasonably ask if the dorsal-ventral differences in the rodent hippocampus can be expected to apply to humans; in humans the ventral region (adjacent to the amygdala) has undergone relatively greater expansion compared to the dorsal portions of the hippocampus [for a review, see Box 1 in Strange et al (2014)]. Functional imaging and lesion data has suggested the posterior hippocampus in humans shows preferential activity during spatial navigation in the nondominant hemisphere (Abrahams et al, 1997;Pu et al, 2017), although this has not reliably been demonstrated for verbal memory tasks in the dominant hemisphere or with intracranial EEG, in which aggregated hippocampal electrodes have been shown to exhibit theta power decreases and gamma band power increases during memory encoding (Sederberg et al, 2007). However, to our knowledge, there has not been a systematic attempt to differentiate anterior and posterior hippocampal electrodes and directly compare oscillatory effects.…”

“…There is an extensive literature describing the memory deficits associated with seizure onset or lesions in either dominant or nondominant hemisphere (Bonelli et al, ; Abrahams et al, ; Pu et al, ). Commensurate with these clinical observations, right lateralized hippocampal oscillations have been observed in humans in spatial memory tasks (Cornwell, Johnson, Holroyd, Carver, & Grillon, ; Ekstrom et al, ; Jacobs et al, ).…”

“…Hemispheric differences in hippocampal activation during mnemonic processing have been observed most strongly in spatial navigation, which is associated with stronger activation effects in the nondominant hemisphere in noninvasive (Abrahams, Pickering, Polkey, & Morris, 1997;Bohbot et al, 1998;Pu, Cornwell, Cheyne, & Johnson, 2017) and invasive studies in humans (Jacobs et al, 2010). Strong lateralization for episodic memory has been less consistently observed in fMRI (Fletcher, Frith, & Rugg, 1997), although structural data (Ezzati et al, 2016) suggest verbal memory stimuli are encoded more strongly in the left hemisphere.…”

Veterans with PTSD demonstrate amygdala hyperactivity while viewing threatening faces: A MEG study

“…Magnetoencephalography (MEG) has excellent temporal specificity, and previous MEG studies using healthy participants have found early amygdala activation in response to emotional faces (Garrido et al, 2012; Garvert et al, 2014; Luo et al, 2007, 2010), consistent with face processing studies that used intracranial recordings (Hesse et al, 2016; Mendez-Bertolo et al, 2016; Pourtois et al, 2010; Sato et al, 2011). Substantial evidence supports the capability of MEG to detect neural activity in deep brain structures (Badura-Brack et al, 2017; Cornwell et al, 2012a, 2012b, 2014; Dalal et al, 2008; McDermott et al, 2016; Proskovec et al, 2016; Pu et al, 2017; Salvadore et al, 2009, 2010; Wilson et al, 2009, 2010, 2011, 2017). One such MEG study used a seed-based functional connectivity approach found that veterans with PTSD had increased functional connectivity relative to veterans without PTSD between the amygdala and ventromedial prefrontal cortex when viewing threatening faces (Dunkley et al, 2016); however, this study did not examine the time course or amplitude or amygdala responses, and thus such data remains unavailable in patients with PTSD.…”

High-gamma activity in the human hippocampus during inter-trial rest periods of a virtual navigation task

“…The environment of each condition in the 6 two training sets was the same, thus the environment in the first training set was 7 defined as new environment and that in the second one as familiar environment. 8 Therefore, the difference between the two training sets allowed us to measure 9 learning of the environment (Pu et al, 2017), and the difference between hidden 10 platform condition and random swimming condition provided an index of 11 goal-directed spatial navigation (Cornwell et al, 2008). To avoid the possibility that 12 environment learning was confounded with learning a specific location, the location 13 of the hidden platform was changed and counterbalanced between the training sets.…”