Anyone who has ever watched a Mafia film is familiar with the scene of a gangster relieving himself with pants pulled to the ankles, as the cubicle door bursts open followed by a barrage of gunfire leaving the gangster blooded and collapsed. During defecation, micturition, grooming, drinking, or eating (or any form of immobility), the neocortex and hippocampus exhibit large amplitude irregular activity (Tehovnik 2017; Vanderwolf 1969) that includes high-frequency ripple discharges associated with the consolidation of declarative memories via the hippocampus and neocortex during wakefulness (Boyce et al. 2016; Canto, De Zeeuw et al. 2017; Dickey et al. 2022; Eichenlaub et al. 2020; Girardeau and Zugaro 2011; Kudrimot and McNaughton 1999; Logothetis et al. 2012; Louie and Wilson 2001; Ólafsdóttir, Carpenter et al. 2017; Rubin et al. 2022).
Ripple discharges in the hippocampus/neocortex are such that there is a replay of previously executed locomotor behavior (for the purpose of memory consolidation of a T-maze, alternation task) both during bouts of immobility at reward delivery (of a grain pellet) and during periods of slow-wave sleep, as studied in Long-Evans rats (Gomperts, Wilson et al. 2015). During immobility at reward, the activity of the ventral tegmental area is coordinated with the hippocampal/neocortical consolidation process. This coordination is absent during sleep. The ventral tegmental reward cells begin to fire as an animal approaches the reward location and then exhibits a vigorous response at the time of reward delivery (this was observed for 20 of 84 ventral tegmental neurons studied). Most significantly, the bursting of the neurons is time locked with the ripple activity that encodes the forward replay of the behavior being executed, i.e., running along a left or right arm of a T-maze for the reward.
As we know, the reward signal is also shared with the inferior olive during periods of immobility and reward delivery, a signal that is responsible for updating learned motor programs at the level of the Purkinje neurons, as mossy fibre discharges representing behavioral context are associated with the reward (during periods of immobility), thereby automating the motor responses (Loyola, De Zeeuw et al. 2019; Marr 1969; Tehovnik, Patel, Tolias et al. 2021). Automation finalizes the learning process, so that the hippocampus and neocortex are free to learn new declarative operations.
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