Synaptic learning rules for sequence learning

Abstract

Remembering the temporal order of a sequence of events is a task easily performed by humans in everyday life, but the underlying neuronal mechanisms are unclear. This problem is particularly intriguing as human behavior often proceeds on a time scale of seconds, which is in stark contrast to the much faster millisecond time-scale of neuronal processing in our brains. One long-held hypothesis in sequence learning suggests that a particular temporal fine-structure of neuronal activity-termed "phase precession"-enables the compression of slow behavioral sequences down to the fast time scale of the induction of synaptic plasticity. Using mathematical analysis and computer simulations, we find that phase precession can improve sequence learning tremendously and that the asymmetric part of the synaptic learning window is essential for temporal-order learning. To test these predictions, we suggest experiments that selectively alter phase precession or the learning window and evaluate memory of temporal order.

Behavior-dependent spatial maps enable efficient theta phase coding

“…In support of this, theta phase precession or theta sequences have been reported for cells responding to elapsed time (Pastalkova et al, 2008;Shimbo et al, 2021), or particular events or behaviors such as jumping , pulling a lever, or sampling an object (Terada et al, 2017;Aronov et al, 2017;Robinson et al, 2017), and has been observed in structures beyond the hippocampus (Kim et al, 2012;Hafting et al, 2008;Jones and Wilson, 2005;van der Meer and Redish, 2011;Tingley et al, 2018;Tang et al, 2021). These findings suggest that the theta phase code plays a role in supporting a wide array of cognitive functions, such as sequential learning (Lisman and Idiart, 1995;Skaggs et al, 1996;Reifenstein et al, 2021), prediction (Lisman and Redish, 2009;Kay et al, 2020) and planning (Johnson and Redish, 2007;Erdem and Hasselmo, 2012;Bolding et al, 2020;Bush et al, 2015).…”

“…These findings suggest that the theta phase code plays a role in supporting a wide array of cognitive functions. In particular, it has been proposed to underlie sequential learning (Lisman and Idiart, 1995;Skaggs et al, 1996;Reifenstein and Kempter, 2020), prediction (Lisman and Redish, 2009;Kay et al, 2020) and action planning (Johnson and Redish, 2007;Erdem and Hasselmo, 2012;Bolding et al, 2019;Bush et al, 2015).…”

Phase precession in the human hippocampus and entorhinal cortex

“…It is important to understand the prevalence of phase precession due to its likely theoretical relevance as neuronal mechanism for binding and compressing sequential events. In brief, phase precession organizes spiking at time intervals below the deactivation time constant of NMDA receptors, facilitating synaptic plasticity between neurons that encode events at behavioral time-scales 7,10,24,[75][76][77] . Strengthening associations between consecutively active neurons may be a widely useful mechanism for learning associations.…”

“…To do this, we measured each neuron's rhythmic frequency of spiking in comparison to the local theta oscillation 49,50 . Identifying a consistent pattern of faster-than-LFP rhythmic spiking would indicate the presence of a precession-like pattern of LFP-coordinated spiking that could bind and compress sequential, non-spatial features of the task -just as spatial phase precession is theorized to do for locations 24,51 .…”

“…Because these neurons spike slightly faster than the theta oscillation as the rodent runs through specific locations, phase precession results in sequences of locations being encoded at different phases of theta oscillations. As such, phase precession may compress spatial trajectories on the scale of behavior into the brief timescale of the theta cycle that is conducive to synaptic plasticity [22][23][24] .…”