The human hippocampus is sensitive to the durations of events and intervals within a sequence

Temporal details are an important facet of our memories for events. Consistent with this, it has been demonstrated that the hippocampus, a key structure in learning and memory, is sensitive to the temporal aspects of event sequences, including temporal order, context, recency and distance. One unexplored issue is whether the hippocampus also responds to the temporal duration characteristics of an event sequence, for example, how long each event lasted for or how much time elapsed between events. To address this, we used a temporal match-mismatch detection paradigm across two functional neuroimaging studies to explore whether the human hippocampus is sensitive to the durations of events and intervals that comprise a sequence lasting on the order of seconds. On each trial participants were shown a series of four scenes during an encoding and a test phase, and had to determine whether the durations of the intervals or events were altered. We observed hippocampal sensitivity to temporal durations within event sequences. Activity was significantly greater when participants detected repeating, in comparison to novel, durations. Moreover, greater functional connectivity was observed between hippocampus and brain regions previously implicated in second and millisecond timing when durations were novel, suggesting that the hippocampus may receive duration information from these areas for use within a mnemonic context rather than generate an independent timing signal. Our novel findings suggest that the hippocampus may integrate temporal duration information when binding event sequences.

[1]  W. Richards,et al.  Time reproductions by H.M. , 1973, Acta psychologica.

[2]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[3]  Lila Davachi,et al.  Similarity Breeds Proximity: Pattern Similarity within and across Contexts Is Related to Later Mnemonic Judgments of Temporal Proximity , 2014, Neuron.

[4]  B. Staresina,et al.  Mind the Gap: Binding Experiences across Space and Time in the Human Hippocampus , 2009, Neuron.

[5]  Emiliano Macaluso,et al.  Functional anatomy of temporal organisation and domain-specificity of episodic memory retrieval , 2012, Neuropsychologia.

[6]  Dominique Hasboun,et al.  Role of the medial temporal lobe in time estimation in the range of minutes , 2007, Neuroreport.

[7]  D. Kumaran,et al.  Novelty signals: a window into hippocampal information processing , 2009, Trends in Cognitive Sciences.

[8]  Andy C. H. Lee,et al.  The hippocampus and visual perception , 2012, Front. Hum. Neurosci..

[9]  Emiliano Macaluso,et al.  Learning about Time: Plastic Changes and Interindividual Brain Differences , 2012, Neuron.

[10]  C. Ranganath,et al.  Prefrontal and Medial Temporal Lobe Activity at Encoding Predicts Temporal Context Memory , 2010, The Journal of Neuroscience.

[11]  Y. Naya,et al.  Integrating What and When Across the Primate Medial Temporal Lobe , 2011, Science.

[12]  N. Burgess,et al.  The hippocampus and memory: insights from spatial processing , 2008, Nature Reviews Neuroscience.

[13]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[14]  J. Aggleton,et al.  The ability of amnesic subjects to estimate time intervals , 1994, Neuropsychologia.

[15]  M. Baulac,et al.  Time estimation in patients with right or left medial-temporal lobe resection , 2001, Neuroreport.

[16]  Raymond P. Kesner,et al.  The role of the hippocampus in memory for the temporal order of a sequence of odors. , 2002 .

[17]  Lila Davachi,et al.  Distinct Memory Signatures in the Hippocampus: Intentional States Distinguish Match and Mismatch Enhancement Signals , 2009, The Journal of Neuroscience.

[18]  Hugo Merchant,et al.  Neural basis of the perception and estimation of time. , 2013, Annual review of neuroscience.

[19]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[20]  A. Yonelinas The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory , 2013, Behavioural Brain Research.

[21]  Benjamin J. Kraus,et al.  Hippocampal “Time Cells”: Time versus Path Integration , 2013, Neuron.

[22]  D. Kumaran,et al.  Match–Mismatch Processes Underlie Human Hippocampal Responses to Associative Novelty , 2007, The Journal of Neuroscience.

[23]  Laurent Hugueville,et al.  Neural network involved in time perception: An fMRI study comparing long and short interval estimation , 2005, Human brain mapping.

[24]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[25]  L. Davachi,et al.  What Constitutes an Episode in Episodic Memory? , 2011, Psychological science.

[26]  E. Maguire,et al.  Newcastle University Eprints , 2022 .

[27]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[28]  David M. Smith,et al.  Hippocampal episode fields develop with learning , 2011, Hippocampus.

[29]  H. Eichenbaum,et al.  Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events , 2011, Neuron.

[30]  Fraser T. Sparks,et al.  Neuronal code for extended time in the hippocampus , 2012, Proceedings of the National Academy of Sciences.

[31]  M. Wittmann The inner sense of time: how the brain creates a representation of duration , 2013, Nature Reviews Neuroscience.

[32]  D. Gaffan,et al.  Impaired Recency Judgments and Intact Novelty Judgments after Fornix Transection in Monkeys , 2004, The Journal of Neuroscience.

[33]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[34]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[35]  Shannon Tubridy,et al.  Medial temporal lobe contributions to episodic sequence encoding. , 2011, Cerebral cortex.

[36]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[37]  Lily Riggs,et al.  The hippocampus supports multiple cognitive processes through relational binding and comparison , 2012, Front. Hum. Neurosci..

[38]  Mingxiong Huang,et al.  Neural representation of interval encoding and decision making. , 2004, Brain research. Cognitive brain research.

[39]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[40]  Roberto Cabeza,et al.  The Short and Long of It: Neural Correlates of Temporal-order Memory for Autobiographical Events , 2008, Journal of Cognitive Neuroscience.

[41]  Roberto Cabeza,et al.  Overlapping Parietal Activity in Memory and Perception: Evidence for the Attention to Memory Model , 2011, Journal of Cognitive Neuroscience.

[42]  Gary H. Glover,et al.  Spiral imaging in fMRI , 2012, NeuroImage.

[43]  J. Lisman,et al.  Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information , 2001, Hippocampus.

[44]  A. R. McIntosh,et al.  Spatiotemporal analysis of event-related fMRI data using partial least squares , 2004, NeuroImage.

[45]  H. Eichenbaum,et al.  Distinct Hippocampal Time Cell Sequences Represent Odor Memories in Immobilized Rats , 2013, The Journal of Neuroscience.

[46]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[47]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

[48]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[49]  Franck Vidal,et al.  Timing, Storage, and Comparison of Stimulus Duration Engage Discrete Anatomical Components of a Perceptual Timing Network , 2008, Journal of Cognitive Neuroscience.

[50]  C R Jack,et al.  Volumetric magnetic resonance imaging. Clinical applications and contributions to the understanding of temporal lobe epilepsy. , 1997, Archives of neurology.

[51]  Matthias J. Gruber,et al.  Hippocampal Activity Patterns Carry Information about Objects in Temporal Context , 2014, Neuron.

[52]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.