Hippocampal CA1 replay becomes less prominent but more rigid without inputs from medial entorhinal cortex

Abstract

The hippocampus is an essential brain area for learning and memory. However, the network mechanisms underlying memory storage, consolidation and retrieval remain incompletely understood. Place cell sequences during theta oscillations are thought to be replayed during non-theta states to support consolidation and route planning. In animals with medial entorhinal cortex (MEC) lesions, the temporal organization of theta-related hippocampal activity is disrupted, which allows us to test whether replay is also compromised. Two different analyses—comparison of co-activation patterns between running and rest epochs and analysis of the recurrence of place cell sequences—reveal that the enhancement of replay by behavior is reduced in MEC-lesioned versus control rats. In contrast, the degree of intrinsic network structure prior and subsequent to behavior remains unaffected by MEC lesions. The MEC-dependent temporal coordination during theta states therefore appears to facilitate behavior-related plasticity, but does not disrupt pre-existing functional connectivity.

The brain in motion: How ensemble fluidity drives memory-updating and flexibility

“…Importantly, the theta phase is critical for determining whether LTP or synaptic depression occurs ( Hyman et al, 2003 ), meaning that not only is the magnitude of theta important, but also the spike timing of neuronal ensembles within theta cycles ( Colgin, 2013 ; Dragoi and Buzsáki, 2006 ). Recent studies have shown that CA1 neuronal spiking needs to be temporally organized within theta cycles in order to be recruited into SPW-R events after learning ( Chenani et al, 2019 ; Dragoi, 2020 ; Drieu et al, 2018 ; Farooq and Dragoi, 2019 ; Farooq et al, 2019 ). Thus, theta oscillations corral ensembles for potentiation and memory-updating.…”

Medial entorhinal cortex lesions induce degradation of CA1 place cell firing stability when self-motion information is used

“…Inactivation of the MEC did not abolish nor dramatically disrupted the spatially selective properties of individual place cell ( Hales et al, 2014 ; Miao et al, 2015 ; Schlesiger et al, 2018 ). They nevertheless altered their remapping characteristics ( Miao et al, 2015 ; Rueckemann et al, 2016 ; see however Schlesiger et al, 2018 ) and the temporal organisation of theta-related hippocampal firing patterns ( Chenani et al, 2019 ; Schlesiger et al, 2015 ).…”

A Model for Navigation in Unknown Environments Based on a Reservoir of Hippocampal Sequences

“…A potential criticism to the model arises from physiological reports that offline sequences are plastic and change from preplay to replay mostly by adding new neurons (Grosmark and Buzsaki 2016;Liu et al 2018a;Chenani et al 2019), whereas in the present model the sequences remain fixed. There are two ways to explain sequence plasticity in the realm of this model.…”

“…In the standard version of the model sequences are replayed serially after each trial in the same order as they have been activated during the search. However, physiological evidence suggests that sequences are plastic in the sense that sequences observed at reward sites have additional neurons included as compared to preplay sequences (Grosmark and Buzsaki 2016;Liu et al 2018a;Chenani et al 2019).…”

“…An alternative idea to utilize internal dynamics for mapping topological spaces is motivated by extensive reports of hippocampal sequences that are present during locomotion in real and abstract spaces (theta sequences) (Foster and Wilson 2007;Aronov et al 2017), during wheel running (Nadasdy et al 1999;Pastalkova et al 2008;Malvache et al 2016), and even during offline states (sequence replay) (Lee and Wilson 2002;Davidson et al 2009;Diba and Buzsaki 2007). Most notably, sequence-like activity patterns were reported to have marked similarity between navigation behavior and offline periods that occur even before the animal navigated a new path (linking of separate experiences) (Gupta et al 2010), or even a whole new maze for the first time (preplay of future events) Tonegawa 2011, 2013;Grosmark and Buzsaki 2016;Liu et al 2018b;Chenani et al 2019).…”