Hippocampus, time, and memory—A retrospective analysis.

Abstract

In 1984, there was considerable evidence that the hippocampus was important for spatial learning and some evidence that it was also involved in duration discrimination. The article Hippocampus, Time, and Memory (Meck, Church, and Olton, 1984), however, was the first to isolate the effects of hippocampal damage on specific stages of temporal processing. In this review, to celebrate the 30th anniversary of Behavioral Neuroscience, we look back on factors that contributed to the long-lasting influence of this article. The major results were that a fimbria-fornix lesion (a) interferes with the ability to retain information in temporal working memory and (b) distorts the content of temporal reference memory, but (c) it did not decrease sensitivity to signal duration. This was the first lesion experiment in which the results were interpreted by a well-developed theory of behavior (scalar timing theory). It has led to extensive research on the role of the hippocampus in temporal processing by many investigators. The most important ones are the development of computational models with plausible neural mechanisms (such as the Striatal Beat-Frequency model of interval timing), the use of multiple behavioral measures of timing, and empirical research on the neural mechanisms of timing and temporal memory using ensemble recording of neurons in prefrontal-striatal-hippocampal circuits.

Comparison of interval timing behaviour in mice following dorsal or ventral hippocampal lesions with mice having δ -opioid receptor gene deletion

“…Importantly, both pre-training and post-training DH lesions produced leftward shifts in peak times, confirming previous investigations and suggesting a possible role for the DH in the cortical-striatal-based timing mechanisms [16,20,22,23,25,70]. Importantly, examination of the individual-trial performance revealed that earlier 'start' times rather than earlier 'stop' times or a combination of both could well be the reason for the observed leftward shifts of peak times.…”

“…fimbria-fornix lesions or complete hippocampal cytotoxic lesions) responded earlier than the scheduled time of reinforcement in a variety of peak-interval procedures [20,68], suggesting that the hippocampus plays a role in temporal memory [25]. Hippocampal lesions also disrupt responding in differential reinforcement of low rates (DRL) schedules.…”

“…Because the behavioural phenotype of these CHL1-deficient mice displays some of the qualitative (e.g. under-reproduction) changes observed in interval timing following DH lesions [25,87], we considered it important to establish additional parallels between alterations in gene expression and selective changes in hippocampalstriatal interactions that might alter interval timing in the multiseconds range.…”

“…Since the initial evaluation of the effects of post-training fimbria-fornix lesions on timing and temporal memory [20], studies investigating the role of the hippocampus in the temporal control of behaviour have generated consistent, though not always conclusive, results [21][22][23][24]. Specifically, both humans and rodents with a variety of different types of hippocampal lesions have been shown to underestimate target durations, and/or to exhibit increased sensitivity to signal duration [25,26]. However, to date, no studies have examined the concurrent timing of multiple target durations as a function of pre-training lesions to the dorsal hippocampus (DH) or ventral hippocampus (VH).…”

Subjective Duration as a Signature of Coding Efficiency: Emerging Links Among Stimulus Repetition, Predictive Coding, and Cortical GABA Levels

“…Meck and colleagues (Allman et al, 2014;Coull et al, 2011; in press b; Lewis & Meck, 2012;MacDonald et al, 2014;Matell & Meck, 2000Meck et al, 2008Meck et al, , 2013Merchant et al, 2013;Van Rijn et al, in press) have proposed a unified timing model in which the perception and estimation of time depends on the interaction of multiple brain areas as outlined in Figure 1. These include structures that are consistently involved in temporal processing across different timing contexts, comprising a core-timing network, as well as areas that are activated in a context-dependent/sensory-specific fashion (e.g., visual cortex or cerebellum -see Chen & Zhou, 2014;Teki et al, 2012 - Fig.…”