Hippocampal place cell encoding of sloping terrain

Effective navigation relies on knowledge of one's environment. A challenge to effective navigation is accounting for the time and energy costs of routes. Irregular terrain in ecological environments poses a difficult navigational problem as organisms ought to avoid effortful slopes to minimize travel costs. Route planning and navigation have previously been shown to involve hippocampal place cells and their ability to encode and store information about an organism's environment. However, little is known about how place cells may encode the slope of space and associated energy costs as experiments are traditionally carried out in flat, horizontal environments. We set out to investigate how dorsal‐CA1 place cells in rats encode systematic changes to the slope of an environment by tilting a shuttle box from flat to 15 ° and 25 ° while minimizing external cue change. Overall, place cell encoding of tilted space was as robust as their encoding of flat ground as measured by traditional place cell metrics such as firing rates, spatial information, coherence, and field size. A large majority of place cells did, however, respond to slope by undergoing partial, complex remapping when the environment was shifted from one tilt angle to another. The propensity for place cells to remap did not, however, depend on the vertical distance the field shifted. Changes in slope also altered the temporal coding of information as measured by the rate of theta phase precession of place cell spikes, which decreased with increasing tilt angles. Together these observations indicate that place cells are sensitive to relatively small changes in terrain slope and that terrain slope may be an important source of information for organizing place cell ensembles. The terrain slope information encoded by place cells could be utilized by efferent regions to determine energetically advantageous routes to goal locations.

[1]  David K Bilkey,et al.  Neurons in the Rat Anterior Cingulate Cortex Dynamically Encode Cost–Benefit in a Spatial Decision-Making Task , 2010, The Journal of Neuroscience.

[2]  I. Whishaw,et al.  Variation in visual acuity within pigmented, and between pigmented and albino rat strains , 2002, Behavioural Brain Research.

[3]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[4]  D. Tank,et al.  Context-Invariant Encoding of Reward Location in a Distinct Hippocampal Population , 2017, bioRxiv.

[5]  Jeanine K. Stefanucci,et al.  Distances appear different on hills , 2005, Perception & psychophysics.

[6]  J. Knierim,et al.  Coming up: in search of the vertical dimension in the brain , 2011, Nature Neuroscience.

[7]  H. Yamahachi,et al.  Hippocampal Remapping after Partial Inactivation of the Medial Entorhinal Cortex , 2015, Neuron.

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

[9]  R. Margaria,et al.  Energy cost of running. , 1963, Journal of applied physiology.

[10]  Kate J. Jeffery,et al.  Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding , 2015, Front. Psychol..

[11]  A. Treves,et al.  Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1 , 2004, Science.

[12]  Jeanine K. Stefanucci,et al.  The Role of Effort in Perceiving Distance , 2003, Psychological science.

[13]  R. Kram,et al.  Applying the cost of generating force hypothesis to uphill running , 2014, PeerJ.

[14]  David K Bilkey,et al.  Neural encoding of competitive effort in the anterior cingulate cortex , 2012, Nature Neuroscience.

[15]  K. Deisseroth,et al.  Place field assembly distribution encodes preferred locations , 2017, PLoS biology.

[16]  Philip Scarf Route choice in mountain navigation, Naismith's rule, and the equivalence of distance and climb , 2007, Journal of sports sciences.

[17]  Matthew A Wilson,et al.  Slow-γ Rhythms Coordinate Cingulate Cortical Responses to Hippocampal Sharp-Wave Ripples during Wakefulness. , 2015, Cell reports.

[18]  J. Taube Head direction cells and the neurophysiological basis for a sense of direction , 1998, Progress in Neurobiology.

[19]  Bruce L. McNaughton,et al.  An Information-Theoretic Approach to Deciphering the Hippocampal Code , 1992, NIPS.

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

[21]  Howard Eichenbaum,et al.  Distinct Pathways for Rule-Based Retrieval and Spatial Mapping of Memory Representations in Hippocampal Neurons , 2013, The Journal of Neuroscience.

[22]  J. Taube,et al.  Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input , 1997, The Journal of Neuroscience.

[23]  N. Ulanovsky,et al.  Hippocampal cellular and network activity in freely moving echolocating bats , 2007, Nature Neuroscience.

[24]  B. McNaughton,et al.  Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. , 1998, Journal of neurophysiology.

[25]  B. Morio,et al.  Comparison of oxygen consumption in rats during uphill (concentric) and downhill (eccentric) treadmill exercise tests. , 2014, Journal of sports science & medicine.

[26]  Kathryn J Jeffery,et al.  Navigating in a three-dimensional world. , 2013, The Behavioral and brain sciences.

[27]  Y. Dan,et al.  Spike Timing-Dependent Plasticity of Neural Circuits , 2004, Neuron.

[28]  J. Taube,et al.  Hippocampal spatial representations require vestibular input , 2002, Hippocampus.

[29]  Matthew A. Wilson,et al.  Cingulate-Hippocampus Coherence and Trajectory Coding in a Sequential Choice Task , 2013, Neuron.

[30]  S. Molden,et al.  Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task , 2001, The Journal of Neuroscience.

[31]  R. Muller,et al.  The firing of hippocampal place cells predicts the future position of freely moving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  A. Minetti,et al.  Energy cost of walking and running at extreme uphill and downhill slopes. , 2002, Journal of applied physiology.

[33]  Jakob N. Foerster,et al.  Three-dimensional head-direction coding in the bat brain , 2014, Nature.

[34]  W. Epstein,et al.  Perceiving Distance: A Role of Effort and Intent , 2004, Perception.

[35]  B L McNaughton,et al.  Hippocampal place-cell firing during movement in three-dimensional space. , 2001, Journal of neurophysiology.

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

[37]  H. Eichenbaum Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[38]  A Berthoz,et al.  Inertial, Substratal and Landmark Cue Control of Hippocampal CA1 Place Cell Activity , 1995, The European journal of neuroscience.

[39]  Noah A. Russell,et al.  The effects of vestibular lesions on hippocampal function in rats , 2005, Progress in Neurobiology.

[40]  J. Knierim,et al.  Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. , 2011, Physiological reviews.

[41]  G. Brooks,et al.  Determination of metabolic and heart rate responses of rats to treadmill exercise. , 1978, Journal of applied physiology: respiratory, environmental and exercise physiology.

[42]  Francesco Savelli,et al.  Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. , 2010, Journal of neurophysiology.

[43]  Nachum Ulanovsky,et al.  Representation of Three-Dimensional Space in the Hippocampus of Flying Bats , 2013, Science.

[44]  Sen Cheng,et al.  The transformation from grid cells to place cells is robust to noise in the grid pattern , 2014, Hippocampus.

[45]  M. Moser,et al.  A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation , 2015, Nature.

[46]  K. Jeffery,et al.  Dissociation of the geometric and contextual influences on place cells , 2003, Hippocampus.

[47]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[49]  David K Bilkey,et al.  A low cost, high precision subminiature microdrive for extracellular unit recording in behaving animals , 1999, Journal of Neuroscience Methods.

[50]  Nachum Ulanovsky,et al.  Neuroscience: How Is Three-Dimensional Space Encoded in the Brain? , 2011, Current Biology.

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

[52]  David M. Smith,et al.  Hippocampal place cells, context, and episodic memory , 2006, Hippocampus.

[53]  Noah A. Russell,et al.  Long-Term Effects of Permanent Vestibular Lesions on Hippocampal Spatial Firing , 2003, The Journal of Neuroscience.

[54]  Jozsef Csicsvari,et al.  Behavioral / Systems / Cognitive Hippocampal Place Cells Can Encode Multiple Trial-Dependent Features through Rate Remapping , 2012 .

[55]  B. McNaughton,et al.  Place field expansion after focal MEC inactivations is consistent with loss of Fourier components and path integrator gain reduction , 2015, Proceedings of the National Academy of Sciences.

[56]  Douglas G Wallace,et al.  Vestibular Information Is Required for Dead Reckoning in the Rat , 2002, The Journal of Neuroscience.

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

[58]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[59]  Brad E. Pfeiffer,et al.  Reverse Replay of Hippocampal Place Cells Is Uniquely Modulated by Changing Reward , 2016, Neuron.

[60]  K. Jeffery,et al.  A role for terrain slope in orienting hippocampal place fields , 2006, Experimental Brain Research.

[61]  J. Taube,et al.  On the nature of three‐dimensional encoding in the cognitive map: Commentary on Hayman, Verriotis, Jovalekic, Fenton, and Jeffery , 2013, Hippocampus.

[62]  C. R. Taylor,et al.  Metabolism of rats running up and down an incline. , 1983, Journal of applied physiology: respiratory, environmental and exercise physiology.

[63]  Douglas A Nitz,et al.  Anterior cingulate neurons in the rat map anticipated effort and reward to their associated action sequences. , 2012, Journal of neurophysiology.

[64]  H. Eichenbaum,et al.  Interplay of Hippocampus and Prefrontal Cortex in Memory , 2013, Current Biology.

[65]  Anthony Di Fiore,et al.  Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications , 2007, Animal Cognition.

[66]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  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.

[68]  Edward S Boyden,et al.  Transient optogenetic inactivation of the medial entorhinal cortex biases the active population of hippocampal neurons , 2016, Hippocampus.

[69]  W E Skaggs,et al.  The Effect of Aging on Experience-Dependent Plasticity of Hippocampal Place Cells , 1997, The Journal of Neuroscience.

[70]  Neil Burgess,et al.  What do grid cells contribute to place cell firing? , 2014, Trends in Neurosciences.

[71]  K. Jeffery,et al.  Anisotropic encoding of three-dimensional space by place cells and grid cells , 2011, Nature Neuroscience.

[72]  J. Wall,et al.  Elephants avoid costly mountaineering , 2006, Current Biology.

[73]  Paul F. Smith,et al.  Vestibular–hippocampal interactions , 1997, Hippocampus.

[74]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[75]  Richard Kempter,et al.  Quantifying circular–linear associations: Hippocampal phase precession , 2012, Journal of Neuroscience Methods.

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

[77]  J. Taube,et al.  Firing Properties of Rat Lateral Mammillary Single Units: Head Direction, Head Pitch, and Angular Head Velocity , 1998, The Journal of Neuroscience.

[78]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[79]  H. Eichenbaum,et al.  Robust Conjunctive Item–Place Coding by Hippocampal Neurons Parallels Learning What Happens Where , 2009, The Journal of Neuroscience.

[80]  André A. Fenton,et al.  Understanding hippocampal activity by using purposeful behavior: Place navigation induces place cell discharge in both task-relevant and task-irrelevant spatial reference frames , 2000 .

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

[82]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

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

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

[85]  Margaret F. Carr,et al.  Hippocampal SWR Activity Predicts Correct Decisions during the Initial Learning of an Alternation Task , 2013, Neuron.