Hippocampal-striatal functional connectivity supports processing of temporal expectations from associative memory

Abstract

<jats:title>Abstract</jats:title><jats:p>The hippocampus and dorsal striatum are both associated with temporal processing, but they are thought to play distinct roles. The hippocampus has been reported to contribute to storing temporal structure of events in memory, whereas the striatum contributes to temporal motor preparation and reward anticipation. Here, we asked whether the striatum cooperates with the hippocampus in processing the temporal context of memorized visual associations. In our task, participants were trained to implicitly form temporal expectations for one of two possible time intervals associated to specific cue-target associations, and subsequently were scanned using 7T functional magnetic resonance imaging. During scanning, learned temporal expectations could be violated when the pairs were presented at either the learned or not-learned time intervals. When temporal expectations were not met during testing trials, activity in hippocampal subfields CA3/CA2 and CA1 decreased while right putamen activity increased, compared to when temporal expectations were met. Further, psycho-physiological interactions showed that functional connectivity between left CA1 and caudate, as well as between putamen and caudate, decreased when temporal expectations were not met. Our results indicate that the hippocampus and striatum cooperate to process implicit temporal expectation from mnemonic associations, with different but complementary contributions from caudate and putamen. Our findings provide further support for a hippocampal-striatal network in temporal associative processing.</jats:p>

Rapid encoding of task regularities in the human hippocampus guides sensorimotor timing

“…This could explain the activity co-fluctuations we observed in our data (Fig. 2C), which fits to prior observations of the two areas interacting in many tasks including associative learning (Mattfeld & Stark, 2015) and navigation (Brown & Stern, 2014), even showing synchronized neural activity in rats (Berke et al, 2004), and when temporal expectations are violated (van de Ven et al, 2020).…”

Selective neural coding of object, feature, and geometry spatial cues in humans

“…There is long-standing knowledge from rodent studies that the hippocampus mediates the formation of cognitive map-like representations (i.e., place-based strategies) while the striatum is specifically involved with stimulus-outcome associations (i.e., response-based strategies) (Squire, 2004; White & McDonald, 2002). Yet, converging evidence from the animal and human literature supports intricate cooperation and competition between these two memory systems (Gahnstrom & Spiers, 2020; Packard & Goodman, 2013; Rinaldi et al, 2020; van de Ven et al, 2020). Critically, Packard and Goodman (2013) posited that the heterogeneity of the visual environment, defined by the presence of multiple visual cues, could modulate this competition by favoring one type of strategy over another, ultimately diminishing competitive interference.…”

“…There is long-standing knowledge from rodent studies that the hippocampus mediates the formation of cognitive map-like representations (i.e., place-based strategies) while the striatum is specifically involved with stimulus-outcome associations (i.e., response-based strategies) [99,100]. Yet, converging evidence from the animal and human literature supports intricate cooperation and competition between these two memory systems [25,101,102].…”

Subcortical Contributions to the Uniqueness of Human Cognition

“…For example, the hippocampus and the striatum (a subregion of the basal ganglia) were reported to be jointly involved in episodic memory encoding (Sadeh et al 2011). Increased functional connectivity between the hippocampus and striatum was also found in learning temporal associations (van de Ven et al 2020). Their interactions also contribute to arbitrary associative learning (Mattfeld & Stark 2015).…”