Human hippocampal theta oscillations reflect sequential dependencies during spatial planning

Movement-related theta oscillations in rodent hippocampus coordinate ‘forward sweeps’ of location-specific neural activity that could be used to evaluate spatial trajectories online. This raises the possibility that increases in human hippocampal theta power accompany the evaluation of upcoming spatial choices. To test this hypothesis, we measured neural oscillations during a spatial planning task that closely resembles a perceptual decision-making paradigm. In this task, participants searched visually for the shortest path between a start and goal location in novel mazes that contained multiple choice points, and were subsequently asked to make a spatial decision at one of those choice points. We observed ~4-8 Hz hippocampal/medial temporal lobe theta power increases specific to sequential planning that were negatively correlated with subsequent decision speed, where decision speed was inversely correlated with choice accuracy. These results implicate the hippocampal theta rhythm in decision tree search during planning in novel environments.

[1]  Adam Johnson,et al.  Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point , 2007, The Journal of Neuroscience.

[2]  Kevin J. Miller,et al.  Dorsal hippocampus contributes to model-based planning , 2017, Nature Neuroscience.

[3]  Christian F. Doeller,et al.  Medial prefrontal theta phase coupling during spatial memory retrieval , 2014, Hippocampus.

[4]  J. Jacobs Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  Tobias Staudigl,et al.  Hexadirectional Modulation of High-Frequency Electrophysiological Activity in the Human Anterior Medial Temporal Lobe Maps Visual Space , 2018, Current Biology.

[6]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[7]  Jean Gotman,et al.  Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation , 2017, Nature Communications.

[8]  I. C. Whitfield,et al.  Chapter 5 – THE NEURAL CODE , 1978 .

[9]  G. Nolte The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. , 2003, Physics in medicine and biology.

[10]  M. A. MacIver,et al.  Massive increase in visual range preceded the origin of terrestrial vertebrates , 2017, Proceedings of the National Academy of Sciences.

[11]  R. Dolan,et al.  Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model , 2017, The Journal of Neuroscience.

[12]  Karl J. Friston,et al.  Planning and navigation as active inference , 2017, Biological Cybernetics.

[13]  Ari Weinstein,et al.  Model-based hierarchical reinforcement learning and human action control , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  Milan Sonka,et al.  3D Slicer as an image computing platform for the Quantitative Imaging Network. , 2012, Magnetic resonance imaging.

[15]  Christian F. Doeller,et al.  Hippocampal-Prefrontal Theta Oscillations Support Memory Integration , 2016, Current Biology.

[16]  Christian F. Doeller,et al.  Movement-Related Theta Rhythm in Humans: Coordinating Self-Directed Hippocampal Learning , 2012, PLoS biology.

[17]  Zahra M. Aghajan,et al.  Theta Oscillations in the Human Medial Temporal Lobe during Real-World Ambulatory Movement , 2016, Current Biology.

[18]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[19]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[20]  Jonathan Miller,et al.  Phase-tuned neuronal firing encodes human contextual representations for navigational goals , 2017, bioRxiv.

[21]  Karl J. Friston,et al.  The Neural Representation of Prospective Choice during Spatial Planning and Decisions , 2017, PLoS biology.

[22]  Tobias Navarro Schröder,et al.  Grid-cell representations in mental simulation , 2016, eLife.

[23]  Simon Hanslmayr,et al.  Human Hippocampal Dynamics during Response Conflict , 2015, Current Biology.

[24]  M. Kahana,et al.  Human hippocampal theta oscillations and the formation of episodic memories , 2012, Hippocampus.

[25]  E. Düzel,et al.  Medial temporal theta state before an event predicts episodic encoding success in humans , 2009, Proceedings of the National Academy of Sciences.

[26]  Neil Burgess,et al.  Forward and Backward Inference in Spatial Cognition , 2013, PLoS Comput. Biol..

[27]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[28]  David J. Foster,et al.  Memory and Space: Towards an Understanding of the Cognitive Map , 2015, The Journal of Neuroscience.

[29]  Neil Burgess,et al.  Medial Prefrontal–Medial Temporal Theta Phase Coupling in Dynamic Spatial Imagery , 2017, Journal of Cognitive Neuroscience.

[30]  Emily Szkudlarek,et al.  Dissociation between Dorsal and Ventral Hippocampal Theta Oscillations during Decision-Making , 2013, The Journal of Neuroscience.

[31]  Christian F. Doeller,et al.  The Role of Mental Maps in Decision-Making , 2017, Trends in Neurosciences.

[32]  R. Dolan,et al.  Synchronization of Medial Temporal Lobe and Prefrontal Rhythms in Human Decision Making , 2013, The Journal of Neuroscience.

[33]  Arne D. Ekstrom,et al.  Human hippocampal theta activity during virtual navigation , 2005, Hippocampus.

[34]  Michael J. Jutras,et al.  Oscillatory activity in the monkey hippocampus during visual exploration and memory formation , 2013, Proceedings of the National Academy of Sciences.

[35]  Gustavo Deco,et al.  Degenerate time-dependent network dynamics anticipate seizures in human epileptic brain , 2017 .

[36]  Zeb Kurth-Nelson,et al.  Fast Sequences of Non-spatial State Representations in Humans , 2016, Neuron.

[37]  Rosa Cossart,et al.  Internally Recurring Hippocampal Sequences as a Population Template of Spatiotemporal Information , 2015, Neuron.

[38]  Kathryn A Davis,et al.  Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation , 2018, Nature Communications.

[39]  A D Redish,et al.  Prediction, sequences and the hippocampus , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  G. Barnes,et al.  Statistical flattening of MEG beamformer images , 2003, Human brain mapping.

[41]  Nathaniel J. Killian,et al.  A map of visual space in the primate entorhinal cortex , 2012, Nature.

[42]  Arne D. Ekstrom,et al.  Behavioral correlates of human hippocampal delta and theta oscillations during navigation. , 2011, Journal of neurophysiology.

[43]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

[44]  Nachum Ulanovsky,et al.  Vectorial representation of spatial goals in the hippocampus of bats , 2017, Science.

[45]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[46]  G. Pezzulo,et al.  Internally generated hippocampal sequences as a vantage point to probe future‐oriented cognition , 2017, Annals of the New York Academy of Sciences.

[47]  Arne D. Ekstrom,et al.  The Spectro-Contextual Encoding and Retrieval Theory of Episodic Memory , 2014, Front. Hum. Neurosci..

[48]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[49]  Arne D. Ekstrom,et al.  Oscillations Go the Distance: Low-Frequency Human Hippocampal Oscillations Code Spatial Distance in the Absence of Sensory Cues during Teleportation , 2016, Neuron.

[50]  F. Carver,et al.  Human Hippocampal and Parahippocampal Theta during Goal-Directed Spatial Navigation Predicts Performance on a Virtual Morris Water Maze , 2008, The Journal of Neuroscience.

[51]  Andrew M. Wikenheiser,et al.  Hippocampal theta sequences reflect current goals , 2015, Nature Neuroscience.

[52]  M. Botvinick,et al.  The hippocampus as a predictive map , 2016 .

[53]  Karl J. Friston,et al.  The Functional Anatomy of Time: What and When in the Brain , 2016, Trends in Cognitive Sciences.

[54]  P. Dayan,et al.  Adaptive integration of habits into depth-limited planning defines a habitual-goal–directed spectrum , 2016, Proceedings of the National Academy of Sciences.

[55]  Emrah Düzel,et al.  Hippocampal Theta-Phase Modulation of Replay Correlates with Configural-Relational Short-Term Memory Performance , 2011, The Journal of Neuroscience.

[56]  Arne D. Ekstrom,et al.  Frequency–specific network connectivity increases underlie accurate spatiotemporal memory retrieval , 2013, Nature Neuroscience.

[57]  S. Hanslmayr,et al.  Theta Oscillations at Encoding Mediate the Context-Dependent Nature of Human Episodic Memory , 2013, Current Biology.

[58]  Mehdi Keramati,et al.  Flexibility to contingency changes distinguishes habitual and goal-directed strategies in humans , 2017, bioRxiv.

[59]  Dmitriy Aronov,et al.  Mapping of a non-spatial dimension by the hippocampal/entorhinal circuit , 2017, Nature.

[60]  S. Becker,et al.  Remembering the past and imagining the future: a neural model of spatial memory and imagery. , 2007, Psychological review.

[61]  Andrew C. Heusser,et al.  Episodic sequence memory is supported by a theta-gamma phase code , 2016, Nature Neuroscience.

[62]  Lily Riggs,et al.  Hippocampal and neocortical oscillatory contributions to visuospatial binding and comparison. , 2013, Journal of experimental psychology. General.

[63]  Dimitri M. Kullmann,et al.  Oscillatory multiplexing of population codes for selective communication in the mammalian brain , 2014, Nature Reviews Neuroscience.

[64]  Adriano B. L. Tort,et al.  Increase in hippocampal theta oscillations during spatial decision making , 2014, Hippocampus.

[65]  Neil Burgess,et al.  Grid-like Processing of Imagined Navigation , 2016, Current Biology.

[66]  N. Burgess,et al.  Human hippocampal theta power indicates movement onset and distance travelled , 2017, Proceedings of the National Academy of Sciences.

[67]  Shuo Wang,et al.  Encoding of Target Detection during Visual Search by Single Neurons in the Human Brain , 2018, Current Biology.