A map of abstract relational knowledge in the human hippocampal–entorhinal cortex

The hippocampal–entorhinal system encodes a map of space that guides spatial navigation. Goal-directed behaviour outside of spatial navigation similarly requires a representation of abstract forms of relational knowledge. This information relies on the same neural system, but it is not known whether the organisational principles governing continuous maps may extend to the implicit encoding of discrete, non-spatial graphs. Here, we show that the human hippocampal–entorhinal system can represent relationships between objects using a metric that depends on associative strength. We reconstruct a map-like knowledge structure directly from a hippocampal–entorhinal functional magnetic resonance imaging adaptation signal in a situation where relationships are non-spatial rather than spatial, discrete rather than continuous, and unavailable to conscious awareness. Notably, the measure that best predicted a behavioural signature of implicit knowledge and blood oxygen level-dependent adaptation was a weighted sum of future states, akin to the successor representation that has been proposed to account for place and grid-cell firing patterns. DOI: http://dx.doi.org/10.7554/eLife.17086.001

[1]  Axel Cleeremans,et al.  Implicit learning: news from the front , 1998, Trends in Cognitive Sciences.

[2]  Alison R Preston,et al.  Hippocampal contribution to the novel use of relational information in declarative memory , 2004, Hippocampus.

[3]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[4]  Russell A. Epstein,et al.  Distances between Real-World Locations Are Represented in the Human Hippocampus , 2011, The Journal of Neuroscience.

[5]  N. Burgess,et al.  Evidence for holistic episodic recollection via hippocampal pattern completion , 2015, Nature Communications.

[6]  E. Moser,et al.  A manifold of spatial maps in the brain , 2010, Trends in Cognitive Sciences.

[7]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[8]  Peter Dayan,et al.  Improving Generalization for Temporal Difference Learning: The Successor Representation , 1993, Neural Computation.

[9]  Oliver Speck,et al.  The impact of physiological noise correction on fMRI at 7 T , 2011, NeuroImage.

[10]  Timothy E. J. Behrens,et al.  Online evaluation of novel choices by simultaneous representation of multiple memories , 2013, Nature Neuroscience.

[11]  M. Botvinick,et al.  Neural representations of events arise from temporal community structure , 2013, Nature Neuroscience.

[12]  H. Eichenbaum,et al.  Can We Reconcile the Declarative Memory and Spatial Navigation Views on Hippocampal Function? , 2014, Neuron.

[13]  Carol A. Seger,et al.  Implicit learning. , 1994, Psychological bulletin.

[14]  Alexander Mathis,et al.  Connecting multiple spatial scales to decode the population activity of grid cells , 2015, Science Advances.

[15]  Desmond J. Higham,et al.  Network Properties Revealed through Matrix Functions , 2010, SIAM Rev..

[16]  D. Broadbent,et al.  On the Relationship between Task Performance and Associated Verbalizable Knowledge , 1984 .

[17]  D. Shohamy,et al.  Preference by Association: How Memory Mechanisms in the Hippocampus Bias Decisions , 2012, Science.

[18]  D. Kumaran,et al.  An Unexpected Sequence of Events: Mismatch Detection in the Human Hippocampus , 2006, PLoS biology.

[19]  Margaret L. Schlichting,et al.  Learning-related representational changes reveal dissociable integration and separation signatures in the hippocampus and prefrontal cortex , 2015, Nature Communications.

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

[21]  Samuel Gershman,et al.  Predictive representations can link model-based reinforcement learning to model-free mechanisms , 2017, bioRxiv.

[22]  Michele Benzi,et al.  Total communicability as a centrality measure , 2013, J. Complex Networks.

[23]  A. Reber.  Implicit learning and tacit knowledge , 1993 .

[24]  Christian F. Doeller,et al.  Memory hierarchies map onto the hippocampal long axis in humans , 2015, Nature Neuroscience.

[25]  E. Tolman.  Cognitive maps in rats and men. , 1948, Psychological review.

[26]  R. Knight,et al.  The Hippocampus and Entorhinal Cortex Encode the Path and Euclidean Distances to Goals during Navigation , 2014, Current Biology.

[27]  Raymond J. Dolan,et al.  Information theory, novelty and hippocampal responses: unpredicted or unpredictable? , 2005, Neural Networks.

[28]  Ron Meir,et al.  Extracting grid cell characteristics from place cell inputs using non-negative principal component analysis , 2016, eLife.

[29]  Timothy E. J. Behrens,et al.  Organizing conceptual knowledge in humans with a gridlike code , 2016, Science.

[30]  D. Kumaran,et al.  The Emergence and Representation of Knowledge about Social and Nonsocial Hierarchies , 2012, Neuron.

[31]  P. Dayan,et al.  States versus Rewards: Dissociable Neural Prediction Error Signals Underlying Model-Based and Model-Free Reinforcement Learning , 2010, Neuron.

[32]  Nicholas J. Higham,et al.  Matching exponential-based and resolvent-based centrality measures , 2016, J. Complex Networks.

[33]  Lauren V. Kustner,et al.  Shaping of Object Representations in the Human Medial Temporal Lobe Based on Temporal Regularities , 2012, Current Biology.

[34]  Nathaniel D. Daw,et al.  Cortical and Hippocampal Correlates of Deliberation during Model-Based Decisions for Rewards in Humans , 2013, PLoS Comput. Biol..

[35]  Ernesto Estrada,et al.  Communicability in complex networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[36]  M. Botvinick,et al.  The successor representation in human reinforcement learning , 2016, Nature Human Behaviour.

[37]  Howard Eichenbaum,et al.  Ventral Hippocampal Neurons Are Shaped by Experience to Represent Behaviorally Relevant Contexts , 2013, The Journal of Neuroscience.

[38]  Neil Burgess,et al.  Using Grid Cells for Navigation , 2015, Neuron.

[39]  Helen C. Barron,et al.  Repetition suppression: a means to index neural representations using BOLD? , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Nicolas W. Schuck,et al.  Human Orbitofrontal Cortex Represents a Cognitive Map of State Space , 2016, Neuron.

[41]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[42]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[43]  Hugo J Spiers,et al.  A navigational guidance system in the human brain , 2007, Hippocampus.

[44]  D. Hassabis,et al.  A Goal Direction Signal in the Human Entorhinal/Subicular Region , 2015, Current Biology.

[45]  Blake S. Porter,et al.  Hippocampal Representation of Related and Opposing Memories Develop within Distinct, Hierarchically Organized Neural Schemas , 2014, Neuron.

[46]  B. Rossion,et al.  Revisiting Snodgrass and Vanderwart's Object Pictorial Set: The Role of Surface Detail in Basic-Level Object Recognition , 2004, Perception.

[47]  Samuel Gershman,et al.  Design Principles of the Hippocampal Cognitive Map , 2014, NIPS.

[48]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[49]  Alice Alvernhe,et al.  Local remapping of place cell firing in the Tolman detour task , 2011, The European journal of neuroscience.

[50]  S. Heckers,et al.  Hippocampal activation during transitive inference in humans , 2004, Hippocampus.

[51]  Timothy Edward John Behrens,et al.  Two Anatomically and Computationally Distinct Learning Signals Predict Changes to Stimulus-Outcome Associations in Hippocampus , 2016, Neuron.

[52]  Alice Alvernhe,et al.  Different CA1 and CA3 Representations of Novel Routes in a Shortcut Situation , 2008, The Journal of Neuroscience.

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

[54]  A. Reber.  Implicit learning of artificial grammars , 1967 .

[55]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[56]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[57]  M. Shapiro,et al.  A Map for Social Navigation in the Human Brain , 2015, Neuron.

[58]  Yaniv Ziv,et al.  Hippocampal ensemble dynamics timestamp events in long-term memory , 2015, eLife.

[59]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[60]  H. Mittelstaedt,et al.  Homing by path integration in a mammal , 1980, Naturwissenschaften.