Theta sequences are essential for internally generated hippocampal firing fields

Abstract

Sensory cue inputs and memory-related internal brain activities govern the firing of hippocampal neurons, but which specific firing patterns are induced by either of the two processes remains unclear. We found that sensory cues guided the firing of neurons in rats on a timescale of seconds and supported the formation of spatial firing fields. Independently of the sensory inputs, the memory-related network activity coordinated the firing of neurons not only on a second-long timescale, but also on a millisecond-long timescale, and was dependent on medial septum inputs. We propose a network mechanism that might coordinate this internally generated firing. Overall, we suggest that two independent mechanisms support the formation of spatial firing fields in hippocampus, but only the internally organized system supports short-timescale sequential firing and episodic memory.

Time Cells in Hippocampal Area CA3

“…This difference between temporal and spatial representation may be attributable to absence of temporal cues beyond the onset of running in contrast to the prevalence of spatial cues throughout traversal of the maze. This account is consistent with reports that, when environmental cues are reduced, spatial information in place cell activity is diminished (Wang et al, 2015). Increasing field width and decreasing representation over time is a central feature of temporal coding that enables increased efficiency when encoding in a scale invariant manner (Howard et al, 2014).…”

“…This difference in the organization of network coding of time and space is paralleled by a recent observation that, whereas hippocampal time cell representations depend on the theta rhythm, place cell representations do not (Wang et al, 2015). Thus, although time and space coding are very similar in many ways described here, the circuit mechanisms and consequent organization of network representation may be distinct and adaptive to differing demands for internal information processing in the time domain as contrasted with external information processing in the spatial domain.…”

“…The hippocampus plays a critical role in the temporal organization of memories (Eichenbaum, 2014), and a potential mechanism for this temporal organization are hippocampal "time cells," neurons in hippocampal area CA1 that fire at specific moments in temporally structured experiences (Pastalkova et al, 2008;MacDonald et al, 2011Kraus et al, 2013;Modi et al, 2014;Wang et al, 2015). So far, time cells have been examined only in CA1, and it is currently unknown whether other areas of the hippocampus have time cells or where the temporal properties of CA1 time cells originate within the hippocampal circuitry.…”

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

“…Our results demonstrate the modulatory effects of increased neuronal slow oscillations on corticocortical and hippocampal-cortical connectivity. Numerous studies have demonstrated the importance of hippocampal and cortical theta oscillations (4-12 Hz) (60) to coordinate groups of neurons to integrate sensory information (61) and consolidate memory (62,63). Comparatively, our results suggest that the hippocampus plays an even greater role in coordinating brain-wide neural activity, particularly at slow oscillations.…”

Entorhinal–hippocampal neuronal circuits bridge temporally discontiguous events

“…Indeed, CA1 sequential activity is also observed during the delay period of tasks such as the DNTP procedure described earlier; that is, tasks in which rats must alternate between taking different spatial routes on successive trials (Pastalkova et al 2008;Gill et al 2011;Kraus et al 2013,). In a spatial alternation task, it was recently reported that time-cell sequences in the CA1 are profoundly disrupted by temporary inactivation of the medial septum during the delay period and performance was also impaired (Wang et al 2015). Because the medial septum sends diverse and diffuse projections to the HPC and EC (Meibach and Siegel 1977), future work will be needed to tease apart the precise mechanisms at the heart of this disruption.…”