Hippocampal Network Dynamics during Rearing Episodes

Abstract

SummaryAnimals build a model of their surroundings on the basis of information gathered during exploration. Rearing on the hindlimbs changes the vantage point of the animal, increasing the sampled area of the environment. This environmental knowledge is suggested to be integrated into a cognitive map stored by the hippocampus. Previous studies have found that damage to the hippocampus impairs rearing. Here, we characterize the operational state of the hippocampus during rearing episodes. We observe an increase of theta frequency paralleled by a sink in the dentate gyrus and a prominent theta-modulated fast gamma transient in the middle molecular layer. On the descending phase of rearing, a decrease of theta power is detected. Place cells stop firing during rearing, while a different subset of putative pyramidal cells is activated. Our results suggest that the hippocampus switches to a different operational state during rearing, possibly to update spatial representation with information from distant sources.

Different theta frameworks coexist in the hippocampus and are coordinated during memory-guided exploration and novelty detection

“…In contrast to mismatch novelty, uncharted novelty involves the exposure to a previously unvisited context and therefore it lacks a memory representation. Interestingly, a recent study using an uncharted novelty test showed increased theta-gamma CFC exclusively in EC pathways, but not in the CA3→CA1 pathway (Barth et al, 2018). Thus, in the absence of a memory representation, only EC-pathways conveying information about the environmental cues demonstrate enhanced theta-gamma coupling, lending support to our hypothesis.…”

“…Importantly, increased CFC reached significance in the rearing-associated EC pathways (Barth et al, 2018). Overall, the changes found in mismatch novelty cannot be solely explained by the rearing behaviour.…”

“…Overall, the changes found in mismatch novelty cannot be solely explained by the rearing behaviour. Furthermore, we measured theta frequency in the complete time series and compared it between control and novelty conditions, and did not find an increase comparable to unchart noverty (Barth et al, 2018), but rather a significant decrease for Sch-IC and PP-IC theta frequency in t2 ( Figure S6) (Wells et al, 2013). After the habituation period (control), the animals were exposed to a different floor (sand paper) located inside the familiar open field, providing a new tactile stimulus (novelty).…”

“…Thus, in the absence of a memory representation, only EC-pathways conveying information about the environmental cues demonstrate enhanced theta-gamma coupling, lending support to our hypothesis. Furthermore, in the above uncharted novelty study, the authors showed that CFC in EC pathways preferentially occurs when the animal is rearing on its hind legs, an exploratory response to novelty (Lever et al, 2006), which is also associated with increased theta frequency (Barth et al, 2018). To investigate the potential contribution of rearing behaviour to our findings in the mismatch novelty task, we removed from our recordings the epochs in which animals were rearing on their hind legs and then reanalysed ICPC and CFC.…”

‘Awake delta’ and theta-rhythmic hippocampal network modes during intermittent locomotor behaviors in the rat

“…In contrast to delta, the theta rhythm (6-10 Hz) in HC and connected structures is a wellorganized oscillation that is critical for spatial navigation and episodic memory (Winson, 1978, Buzsaki, 2002, Buzsaki & Moser, 2013; shows frequency and power correlations to locomotor speed (Whishaw & Vanderworf, 1973, McFarland et al, 1975, Maurer et al, 2005, Hinman et al, 2016 and behaviors related to active attention and environmental sampling (Aghajan et al, 2017, Barth et al, 2018; exhibits functionally-relevant cross-frequency coupling to gamma oscillations (>25 Hz) (Canolty et al, 2006, Tort et al, 2009, Shirvalkar et al, 2010; and coordinates robust spiking within the HC (Okeefe & Recce, 1993, Foster & Wilson, 2007, Johnson & Redish, 2007, and its projection targets (Sirota et al, 2008, that is critical for learning, decision making, and representations of ongoing, remembered, or imagined future experiences (Richard et al, 2013, Pfeiffer & Foster, 2013, Redish, 2016, Schacter et al, 2007.…”