The cognitive nuances of surprising events: exposure to unexpected stimuli elicits firing variations in neurons of the dorsal CA1 hippocampus

Abstract

The ability to recognize novel situations is among the most fascinating and vital of the brain functions. A hypothesis posits that encoding of novelty is prompted by failures in expectancy, according to computation matching incoming information with stored events. Thus, unexpected changes in context are detected within the hippocampus and transferred to downstream structures, eliciting the arousal of the dopamine system. Nevertheless, the precise locus of detection is a matter of debate. The dorsal CA1 hippocampus (dCA1) appears as an ideal candidate for operating a mismatch computation and discriminating the occurrence of diverse stimuli within the same environment. In this study, we sought to determine dCA1 neuronal firing during the experience of novel stimuli embedded in familiar contexts. We performed population recordings while head-fixed mice navigated virtual environments. Three stimuli were employed, namely a novel pattern of visual cues, an odor, and a reward with enhanced valence. The encounter of unexpected events elicited profound variations in dCA1 that were assessed both as opposite rate directions and altered network connectivity. When experienced in sequence, novel stimuli elicited specific responses that often exhibited cross-sensitization. Short-latency, event-triggered responses were in accordance with the detection of novelty being computed within dCA1. We postulate that firing variations trigger neuronal disinhibition, and constitute a fundamental mechanism in the processing of unexpected events and in learning. Elucidating the mechanisms underlying detection and computation of novelty might help in understanding hippocampal-dependent cognitive dysfunctions associated with neuropathologies and psychiatric conditions.Electronic supplementary materialThe online version of this article (10.1007/s00429-018-1681-6) contains supplementary material, which is available to authorized users.

Differential encoding of place value between the dorsal and intermediate hippocampus

“…It is important to note that the spatial correlation coefficient improved in dHP on day 3 (R = 0.9) compared with day 2 (R = 0.81), whereas it remained at the low level in iHP throughout day 3 (R = 0.82; data not shown). Our findings suggest that the decrease in cross-correlation in the population of place cells in dHP on day 2 could be related to the novelty of the event (i.e., the first experience of reward change), 51 not necessarily tied to motivational significance change as in iHP. When the reward was changed to Cheerios from Froot Loops on days 4 to 5, the spatial correlations between population rate maps remained at lower levels in iHP, but not in dHP (Figure 3D).…”

Pattern Separation Underpins Expectation-Modulated Memory

“…CA1 receives pattern-separated inputs from CA3 and projections from EC, reflecting retrieval of existing representations (Norman and O'Reilly, 2003). Given these connections, CA1 has been postulated to act as a match/mismatch detector (Chen et al, 2011;Elfman et al, 2014;Valenti et al, 2018). CA1 expectation effects are most pronounced at lower levels of perceptual interference (T-F33 overlap) for which PS is not critical.…”

Computational modelling of hippocampal sensitivity to expectation violation

“…CA1 receives pattern-separated inputs from CA3 and projections from EC, reflecting retrieval of existing representations (Norman & O'Reilly, 2003). Given these connections, CA1 has been postulated to act as a match/mismatch detector (Chen, Olsen, Preston, Glover, & Wagner, 2011;Elfman et al, 2014;Valenti, Mikus, & Klausberger, 2018). Our results suggest CA1 representations are indeed sensitive to mismatches, both perceptual and memory-based (Elfman et al, 2014), however, to different extents.…”