Neuronal sequences during theta rely on behavior-dependent spatial maps

Abstract

Navigation through space involves learning and representing relationships between past, current and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations provided by neuronal sequences start behind the animal's true location and then sweep forward. However, the exact relationship between theta phase, represented position and true location remains unclear and even paradoxical. Here, we formalize previous notions of 'spatial' or 'temporal' theta sweeps that have appeared in the literature. We analyze single-cell and population variables in unit recordings from rat CA1 place cells and compare them to model simulations based on each of these schemes. We show that neither spatial nor temporal sweeps quantitatively accounts for how all relevant variables change with running speed. To reconcile these schemes with our observations, we introduce 'behavior-dependent' sweeps, in which theta sweep length and place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. These behavior-dependent spatial maps provide a structured heterogeneity that is essential for understanding the hippocampal code.

The functional role of episodic memory in spatial learning

“…This is because when there is a temporal distance between the agent’s actions and their consequences, the sequential order of past experiences has to be maintained in memory to credit the past states and actions when updating the Q values. The importance of sequentiality is consistent with recent observations that theta sequences in the hippocampus are modulated by the animal’s previous behaviour at the spatial location where the theta sequences occur (Parra-Barrero et al, 2021).…”

Action-driven remapping of hippocampal neuronal populations in jumping rats

“…Our observation that the compression of distance to theta-phase (time) offset between place-cell pairs remained unaltered during jump trials, despite changes in firing patterns of individual place cells, supports the internally organized hippocampal model. Previous experiments also found that theta time offset of spikes between place-cell pairs remains fixed, despite increasing distances between place-field peaks in larger environments ( 2 ), running speed differences ( 83 ), or different temporal requirements ( 84 ). Yet, action- and environment-anchored reference frames can coexist in the hippocampus ( 85 ).…”

Navigation and the Efficiency of Spatial Coding: Insights from Closed-Loop Simulations

“…However, the brain consistently opts for more and smaller fields in certain situations, so this suggests that there are factors beyond the Fisher information that constrain spatial coding in the place cell population. Some variables that might impose additional constraints are the size of obstacles (our simulation did not include any), and temporal coding linked to the behavior of the animal, such as running speed (Parra-Barrero et al, 2021). In addition, there are more generic limitations on efficient coding, i.e.…”

“…Lee, Griffin, Zilli, Eichenbaum, & Hasselmo, 2006; J.S. Lee, Briguglio, Cohen, Romani, & Lee, 2020; Parra-Barrero, Diba, & Cheng, 2021; Sato et al, 2020; Tryon et al, 2017; Turi et al, 2019; Zaremba et al, 2017). The same observation was made near walls as compared to further away Tanni, De Cothi, and Barry (2022).…”