The encoding and storage of experience by the hippocampus is essential for the formation of episodic memories and the transformation of individual experiences into semantic structures such as maps and schemas. The rodent hippocampus compresses ongoing experience into repeating theta sequences, but the factors determining the content of theta sequences are not understood. Here we first show that the spatial paths represented by theta sequences in rats extend farther in front of the rat during acceleration and higher running speeds and begin farther behind the rat during deceleration. Second, the length of the path is directly related to the length of the theta cycle and the number of gamma cycles in it. Finally, theta sequences represent the environment in segments or 'chunks'. These results imply that information encoded in theta sequences is subject to powerful modulation by behavior and task variables. Furthermore, these findings suggest a potential mechanism for the cognitive 'chunking' of experience.
At a glance
- Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, Massachusetts, USA, 1993). &
- The Hippocampus as a Cognitive Map (Clarendon Press, Oxford, UK, 1978). &
- Patients with hippocampal amnesia cannot imagine new experiences. Proc. Natl. Acad. Sci. USA 104, 1726–1731 (2007). , , &
- Remembering the past to imagine the future: the prospective brain. Nat. Rev. Neurosci. 8, 657–661 (2007). , &
- Midbrain dopamine neurons encode decisions for future action. Nat. Neurosci. 9, 1057–1063 (2006). , , , &
- Beyond the Cognitive Map: From Place Cells to Episodic Memory (MIT Press, Cambridge, Massachusetts, USA, 1999).
- Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407–418 (1969).
- Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149–172 (1996). , , &
- Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145–157 (2006). &
- Hippocampal theta sequences. Hippocampus 17, 1093–1099 (2007). &
- Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6, 271–280 (1996). , , &
- Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 3, 279–287 (1996). &
- Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons. Trends Neurosci. 30, 325–333 (2007). &
- Theta phase precession beyond the hippocampus. Rev. Neurosci. 23, 39–65 (2012). , &
- Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993). &
- Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. USA 104, 8149–8154 (2007). , , , &
- Single-trial phase precession in the hippocampus. J. Neurosci. 29, 13232–13241 (2009). et al.
- Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. USA 107, 7957–7962 (2010). et al.
- Hippocampal replay is not a simple function of experience. Neuron 65, 695–705 (2010). , , &
- Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006). &
- Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10, 1241–1242 (2007). &
- Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147–153 (2011). , &
- Behavioral Correlates of Hippocampal Neural Sequences PhD thesis, (Carnegie Mellon Univ, 2011).
- Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176–12189 (2007). &
- Dentate gyrus and CA1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J. Neurosci. 21, 7284–7292 (2001). , , &
- Greater running speeds result in altered hippocampal phase sequence dynamics. Hippocampus 22, 737–747 (2012). , , , &
- Prediction, sequences and the hippocampus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1193–1201 (2009). &
- Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 30, 1777–1787 (2010). , , &
- Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 31, 2843–2854 (2011). &
- Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000). , , &
- Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000). , &
- Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227–1239 (2003). &
- Firing rate dynamics in the hippocampus induced by trajectory learning. J. Neurosci. 28, 4679–4689 (2008). &
- Dissociating the effects of past and future on neural encoding of sequences in the hippocampus. J. Neurosci. 28, 8383–8384 (2008).
- Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827–840 (2005).
- The role of hippocampal regions CA3 and CA1 in matching entorhinal input with retrieval of associations between objects and context: Theoretical comment on Lee et al. (2005). Behav. Neurosci. 119, 342–345 (2005).
- A model of episodic memory: mental time travel along encoded trajectories using grid cells. Neurobiol. Learn. Mem. 92, 559–573 (2009).
- The firing of hippocampal place cells predicts the future position of freely moving rats. J. Neurosci. 9, 4101–4110 (1989). &
- Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J. Neurosci. 24, 4541–4550 (2004). , &
- Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587–594 (2008). , , &
- Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267, 1512–1515 (1995). &
- The theta/gamma discrete phase code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15, 913–922 (2005).
- The magical number seven, plus or minus two: some limits on our capacity for processing information. Psychol. Rev. 63, 81–97 (1956).
- Unified Theories of Cognition (Harvard University Press, 1990).
- Human Problem Solving (Prentice-Hall, Englewood Cliffs, New Jersey, USA, 1972). &
- Neurons in hippocampal afferent zones of rat striatum parse routes into multi-pace segments during maze navigation. Eur. J. Neurosci. 19, 1923–1932 (2004). , &
- Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J. Neurosci. 29, 12597–12605 (2009). &
- Hippocampal replay of extended experience. Neuron 63, 497–507 (2009). , &
- Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. J. Neurosci. 26, 12415–12426 (2006). , &
- Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131, 1–11 (2005). , , , &
- Neuronal activity in the rodent dorsal striatum in sequential navigation: separation of spatial and reward responses on the multiple T task. J. Neurophysiol. 91, 2259–2272 (2004). &
- Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 79, 1017–1044 (1998). , , &
- Discrete-time adaptive windowing for velocity estimation. IEEE Trans. Control Syst. Technol. 8, 1003–1009 (2000). , &
- Supplementary Text and Figures (2 MB)
Supplementary Figures 1–9