Temporal and Rate Coding for Discrete Event Sequences in the Hippocampus

Abstract

Although the hippocampus is critical to episodic memory, neuronal representations supporting this role, especially relating to nonspatial information, remain elusive. Here, we investigated rate and temporal coding of hippocampal CA1 neurons in rats performing a cue-combination task that requires the integration of sequentially provided sound and odor cues. The majority of CA1 neurons displayed sensory cue-, combination-, or choice-specific (simply, "event"-specific) elevated discharge activities, which were sustained throughout the event period. These event cells underwent transient theta phase precession at event onset, followed by sustained phase locking to the early theta phases. As a result of this unique single neuron behavior, the theta sequences of CA1 cell assemblies of the event sequences had discrete representations. These results help to update the conceptual framework for space encoding toward a more general model of episodic event representations in the hippocampus.

Hippocampal ensembles represent sequential relationships among discrete nonspatial events

“…Consistent with previous reports [11][12][13][14] , hippocampal activity showed sequences of firing fields ("time cell" activity) during stimulus presentations (Fig 2b) as well as during intervals between stimulus presentations ( Fig S1). Here we take advantage of our unique behavioral paradigm to extend these findings, by determining how this form of temporal coding interacts with stimulus identity and whether it extends across sequences of stimuli.…”

“…These findings are consistent with, and provide potential neuronal mechanisms for, the critical role of the hippocampus in temporally organizing our past experiences and future behavior. Sequential firing fields ("time cells") have previously been reported during individual stimulus presentations, inter-stimulus intervals, and across contiguous stimuli and responses [11][12][13][14] . Considerable evidence indicates this form of coding can provide a strong temporal signal within such task events 13,14 .…”

“…The emerging conceptual framework suggests that the propensity of the hippocampal network to generate and preserve sequential patterns of activity underlies this fundamental capacity 4, 6-10 , a view supported by two main lines of electrophysiological evidence. First, hippocampal ensemble activity tends to exhibit sequential firing fields during the presentation of individual stimuli or inter-stimulus intervals (also known as "time cell" activity) 11,12 , which has been shown to provide a strong temporal signal within such task events 13,14 . Second, hippocampal neurons have been shown to code for sequences of spatial locations under different experimental conditions 6,15,16 .…”

Brain reflections: A circuit‐based framework for understanding information processing and cognitive control

“…the advantage of digital over analog electronics). Evidence in support of this idea is the observation that activity in the hippocampus, a structure considered crucial for this glueing function (generating relational representations, N. J. Cohen et al, ) is characterized by the presence of a very specific form of rhythmic activity (hippocampal theta; Terada, Sakurai, Nakahara, & Fujisawa, ). Third, it provides for periods of “weak” information maintenance, a feature that may be useful if the current dominant representation needs to be replaced by a new representation (see the notion that alpha gating may resemble an antilock brake system, which can block input processing while providing a mechanism for maintaining some level of contact with the external world; Mathewson et al, ).…”

Space and time in the brain

“…Given the many possible routes, the answers to the question “What is the function of this circuit?” will be very different, depending on the routes the investigator tests in a given experiment. The function may appear to be space (14, 15), time (24), sound frequency (27), odor-sound sequence (60), memory (18), or something else, even though the hippocampus responds to each case by generating ordinal cell assembly sequences relevant to the particular situation (20). These considerations generalize to other brain regions as well (61, 62).…”