Mapping of a non-spatial dimension by the hippocampal/entorhinal circuit

During spatial navigation, neural activity in the hippocampus and the medial entorhinal cortex (MEC) is correlated to navigational variables such as location, head direction, speed, and proximity to boundaries. These activity patterns are thought to provide a map-like representation of physical space. However, the hippocampal–entorhinal circuit is involved not only in spatial navigation, but also in a variety of memory-guided behaviours. The relationship between this general function and the specialized spatial activity patterns is unclear. A conceptual framework reconciling these views is that spatial representation is just one example of a more general mechanism for encoding continuous, task-relevant variables. Here we tested this idea by recording from hippocampal and entorhinal neurons during a task that required rats to use a joystick to manipulate sound along a continuous frequency axis. We found neural representation of the entire behavioural task, including activity that formed discrete firing fields at particular sound frequencies. Neurons involved in this representation overlapped with the known spatial cell types in the circuit, such as place cells and grid cells. These results suggest that common circuit mechanisms in the hippocampal–entorhinal system are used to represent diverse behavioural tasks, possibly supporting cognitive processes beyond spatial navigation.

[1]  J. Kelly,et al.  Auditory sensitivity of the albino rat. , 1976, Journal of comparative and physiological psychology.

[2]  May-Britt Moser,et al.  The entorhinal grid map is discretized , 2012, Nature.

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

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

[5]  Y. Sakurai,et al.  Coding of auditory temporal and pitch information by hippocampal individual cells and cell assemblies in the rat , 2002, Neuroscience.

[6]  G. Buzsáki,et al.  Hippocampal CA1 pyramidal cells form functionally distinct sublayers , 2011, Nature Neuroscience.

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

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

[9]  A. Zador,et al.  Auditory cortex mediates the perceptual effects of acoustic temporal expectation , 2010, Nature Neuroscience.

[10]  M. Moser,et al.  Representation of Geometric Borders in the Entorhinal Cortex , 2008, Science.

[11]  Asohan Amarasingham,et al.  Hippocampus Internally Generated Cell Assembly Sequences in the Rat , 2011 .

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

[13]  B. McNaughton,et al.  Self-Motion and the Hippocampal Spatial Metric , 2005, The Journal of Neuroscience.

[14]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[15]  KiJung Yoon,et al.  Grid Cell Responses in 1D Environments Assessed as Slices through a 2D Lattice , 2016, Neuron.

[16]  Edvard I Moser,et al.  Development of the Spatial Representation System in the Rat , 2010, Science.

[17]  Matthew A. Wilson,et al.  Micro-drive Array for Chronic in vivo Recording: Drive Fabrication , 2009, Journal of visualized experiments : JoVE.

[18]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[19]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[20]  Matthew L. Shapiro,et al.  Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. , 1997 .

[21]  Edvard I. Moser,et al.  Shearing-induced asymmetry in entorhinal grid cells , 2015, Nature.

[22]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

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

[24]  Surya Ganguli,et al.  Environmental Boundaries as an Error Correction Mechanism for Grid Cells , 2015, Neuron.

[25]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[26]  M. Moser,et al.  Understanding memory through hippocampal remapping , 2008, Trends in Neurosciences.

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

[28]  Shumeet Baluja,et al.  Advances in Neural Information Processing , 1994 .

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

[30]  Marc W Howard,et al.  Gradual Changes in Hippocampal Activity Support Remembering the Order of Events , 2007, Neuron.

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

[32]  Lisa M. Giocomo,et al.  Topography of Head Direction Cells in Medial Entorhinal Cortex , 2014, Current Biology.

[33]  John J Hopfield,et al.  Neurodynamics of mental exploration , 2009, Proceedings of the National Academy of Sciences.

[34]  Dmitriy Aronov,et al.  Engagement of Neural Circuits Underlying 2D Spatial Navigation in a Rodent Virtual Reality System , 2014, Neuron.

[35]  Edvard I. Moser,et al.  Speed cells in the medial entorhinal cortex , 2015, Nature.

[36]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

[37]  Caswell Barry,et al.  Grid cell symmetry is shaped by environmental geometry , 2015, Nature.

[38]  Mark P. Brandon,et al.  During Running in Place, Grid Cells Integrate Elapsed Time and Distance Run , 2015, Neuron.

[39]  M. Kuperstein,et al.  Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[41]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.