Bidirectional propagation of low frequency oscillations over the human hippocampal surface

Abstract

The hippocampus is diversely interconnected with other brain systems along its axis. Cycles of theta-frequency activity are believed to propagate from the septal to temporal pole, yet it is unclear how this one-way route supports the flexible cognitive capacities of this structure. We leveraged novel thin-film microgrid arrays conformed to the human hippocampal surface to track neural activity two-dimensionally in vivo. All oscillation frequencies identified between 1–15 Hz propagated across the tissue. Moreover, they dynamically shifted between two roughly opposite directions oblique to the long axis. This predominant propagation axis was mirrored across participants, hemispheres, and consciousness states. Directionality was modulated in a participant who performed a behavioral task, and it could be predicted by wave amplitude topography over the hippocampal surface. Our results show that propagation directions may thus represent distinct meso-scale network computations, operating along versatile spatiotemporal processing routes across the hippocampal body.

The direction and timing of theta and alpha traveling waves modulate human memory processing

“…This interpretation is also consistent with earlier work showing that different patterns of neuronal oscillations modulate feedforward networks during visual perception 51,54 and as well as feedback processing during top-down control and prediction 55 . Consistent with our results, there is also other evidence of neural activity changing direction for specific functional states 25,44,56–60 , thus suggesting that our results are part of a broader phenomenon.…”

“…A key aspect of our results is identifying a link between distinct directions of TW propagation and separate functional processes, in particular memory encoding and recall. In conjunction with earlier research 25,44,45 , this suggests that a fundamental way in which the brain’s functional connectivity transiently reorganizes is by changing the directional interactions between different brain regions. Because posterior-to-anterior TWs were associated with successful memory encoding and anterior-to-posterior TWs were associated with memory recall (Fig.…”

“…In particular, our direction results indicate that measuring TW propagation can indicate whether the current brain state is well suited for memory encoding. Going forward, it may be possible to use TWs to measure more advanced aspects of cognition, perhaps with the use of improved recording methods, including high-density neural recording arrays 44,86,87 , as well as with noninvasive methods 16,88,89 . Further, TWs could provide biomarkers for identifying neurological disorders related to abnormal neural connectivity such as autism 90 or epilepsy 91 .…”

Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves

“…Recent studies in humans suggested that the hierarchical organization of neuronal activity across the cortex is not a stationary phenomenon, rather that it has a dynamic phenomenon, which propagates across the cortex in space and time ( Alamia and VanRullen, 2019 ; Halgren et al, 2019 ; Hangya et al, 2011 ; Kleen et al, 2021 ; Lozano-Soldevilla and VanRullen, 2019 ; Massimini et al, 2004 ; Muller et al, 2016 ; Stolk et al, 2019 ; Zhang and Jacobs, 2015 ; Zhang et al, 2018 ). This phenomenon, also known as ‘traveling waves,’ consists of oscillations that propagate progressively across the cortex.…”

Traveling waves in the monkey frontoparietal network predict recent reward memory

“…TWs have been found in multichannel recordings of local field potentials across multiple animal species, frequencies, brain states, and brain systems, suggesting that they are a widespread feature of neural activity. Importantly, in addition to being found during sleep (Dickey et al, 2021; Massimini et al, 2004; Muller et al, 2016), TWs are prominent during active behaviors in animals – including in the hippocampus of rodents during navigation (Lubenov and Siapas, 2009; Patel et al, 2012), and visual regions of monkeys during perception (Davis et al, 2020, 2021) – as well as in humans performing visual (Alamia and VanRullen, 2019; Alamia et al, 2020; Halgren et al, 2019; Pang et al, 2020) and memory tasks (Kleen et al, 2021; Zhang and Jacobs, 2015; Zhang et al, 2018). In some of these studies, specific TW properties (e.g., strength or direction) correlate with accuracy and reaction times (Balasubramanian et al, 2020; Davis et al, 2020; Zhang et al, 2018) suggesting that TWs are functionally significant in linking neural activity with behavior.…”