Exposure to complex environments results in more sparse representations of space in the hippocampus

The neural circuitry mediating sensory and motor representations is adaptively tuned by an animal's interaction with its environment. Similarly, higher order representations such as spatial memories can be modified by exposure to a complex environment (CE), but in this case the changes in brain circuitry that mediate the effect are less well understood. Here, we show that prolonged CE exposure was associated with increased selectivity of CA1 “place cells” to a particular recording arena compared to a social control (SC) group. Furthermore, fewer CA1 and DG neurons in the CE group expressed high levels of Arc protein, a marker of recent activation, following brief exposure to a completely novel environment. The reduced Arc expression was not attributable to overall changes in cell density or number. These data indicate that one effect of CE exposure is to modify high‐level spatial representations in the brain by increasing the sparsity of population coding within networks of neurons. Greater sparsity could result in a more efficient and compact coding system that might alter behavioural performance on spatial tasks. The results from a behavioural experiment were consistent with this hypothesis, as CE‐treated animals habituated more rapidly to a novel environment despite showing equivalent initial responding.

[1]  Raymond P. Kesner,et al.  Selective lesions of the dentate gyrus produce disruptions in place learning for adjacent spatial locations , 2012, Neurobiology of Learning and Memory.

[2]  Bruno A Olshausen,et al.  Sparse coding of sensory inputs , 2004, Current Opinion in Neurobiology.

[3]  Edmund T. Rolls,et al.  The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain , 1990 .

[4]  F. Gage,et al.  More hippocampal neurons in adult mice living in an enriched environment , 1997, Nature.

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

[6]  F. Ebner,et al.  Experience-dependent plasticity in adult rat barrel cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Muller,et al.  Spatial firing properties of hippocampal theta cells , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[9]  A. Treves,et al.  Hippocampal remapping and grid realignment in entorhinal cortex , 2007, Nature.

[10]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[11]  B. McNaughton,et al.  Replay of Neuronal Firing Sequences in Rat Hippocampus During Sleep Following Spatial Experience , 1996, Science.

[12]  Panayiota Poirazi,et al.  Dendrites of dentate gyrus granule cells contribute to pattern separation by controlling sparsity , 2016, Hippocampus.

[13]  Michael J Eckert,et al.  Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices. , 2010, Learning & memory.

[14]  D. Hubel,et al.  Plasticity of ocular dominance columns in monkey striate cortex. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  E. Schuman,et al.  Dendrites , 1978, Journal of the Geological Society.

[16]  C. Koch,et al.  Sparse Representation in the Human Medial Temporal Lobe , 2006, The Journal of Neuroscience.

[17]  T. Foster,et al.  Mechanism for increased hippocampal synaptic strength following differential experience. , 2001, Journal of neurophysiology.

[18]  Adam Santoro,et al.  Reassessing pattern separation in the dentate gyrus , 2013, Front. Behav. Neurosci..

[19]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 2004, Experimental Brain Research.

[20]  T. Wiesel Postnatal development of the visual cortex and the influence of environment , 1982, Nature.

[21]  D. W. In memory of ... , 1963, Science.

[22]  F. Gage,et al.  Neural consequences of enviromental enrichment , 2000, Nature Reviews Neuroscience.

[23]  R. Wurtman,et al.  Environmental conditions influence hippocampus‐dependent behaviours and brain levels of amyloid precursor protein in rats , 2002, The European journal of neuroscience.

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

[25]  Carol A Barnes,et al.  Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites , 1995, Neuron.

[26]  V. Brown,et al.  Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats , 2004, Behavioural Brain Research.

[27]  Patricia E. Sharp,et al.  Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: Comparison with hippocampal place cells , 1997, Behavioural Brain Research.

[28]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[29]  K. Jeffery,et al.  A proposed architecture for the neural representation of spatial context , 2004, Neuroscience & Biobehavioral Reviews.

[30]  J. B. Ranck,et al.  Electrophysiological characteristics of hippocampal complex-spike cells and theta cells , 2004, Experimental Brain Research.

[31]  P. E. Sharp Subicular place cells generate the same “map” for different environments: Comparison with hippocampal cells , 2006, Behavioural Brain Research.

[32]  R. C. Tees The influences of rearing environment and neonatal choline dietary supplementation on spatial learning and memory in adult rats , 1999, Behavioural Brain Research.

[33]  Diano F. Marrone,et al.  Immediate-Early Gene Expression at Rest Recapitulates Recent Experience , 2008, The Journal of Neuroscience.

[34]  B. McNaughton,et al.  Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience , 2005, Hippocampus.

[35]  Ila R Fiete,et al.  Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong. , 2004, Journal of neurophysiology.

[36]  May-Britt Moser,et al.  Place cells, spatial maps and the population code for memory , 2005, Current Opinion in Neurobiology.

[37]  F. Volkmar,et al.  Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. , 1973, Experimental neurology.

[38]  Mattias P. Karlsson,et al.  Network Dynamics Underlying the Formation of Sparse, Informative Representations in the Hippocampus , 2008, The Journal of Neuroscience.

[39]  Carol A Barnes,et al.  Spatial Exploration-Induced Arc mRNA and Protein Expression: Evidence for Selective, Network-Specific Reactivation , 2005, The Journal of Neuroscience.

[40]  P E Sharp,et al.  Subicular place cells expand or contract their spatial firing pattern to fit the size of the environment in an open field but not in the presence of barriers: comparison with hippocampal place cells. , 1999, Behavioral neuroscience.

[41]  Hartwig R. Siebner,et al.  Sparse encoding of automatic visual association in hippocampal networks , 2014, NeuroImage.

[42]  R. Muller,et al.  Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli , 2000, The Journal of general physiology.

[43]  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.

[44]  James J Knierim,et al.  Dynamic Interactions between Local Surface Cues, Distal Landmarks, and Intrinsic Circuitry in Hippocampal Place Cells , 2002, The Journal of Neuroscience.

[45]  Doyun Lee,et al.  Hippocampal Place Fields Emerge upon Single-Cell Manipulation of Excitability During Behavior , 2012, Science.

[46]  W. Greenough,et al.  Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[47]  H. C. LONGUET-HIGGINS,et al.  Non-Holographic Associative Memory , 1969, Nature.

[48]  Terrence J. Sejnowski,et al.  Neuronal Tuning: To Sharpen or Broaden? , 1999, Neural Computation.

[49]  R. Muller,et al.  A Quarter of a Century of Place Cells , 1996, Neuron.

[50]  Nandor Ludvig Place Cells Can Flexibly Terminate and Develop Their Spatial Firing. A New Theory for Their Function , 1999, Physiology & Behavior.

[51]  M. Andersson,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005 .

[52]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[53]  D. Bilkey,et al.  Instability in the Place Field Location of Hippocampal Place Cells after Lesions Centered on the Perirhinal Cortex , 2001, The Journal of Neuroscience.

[54]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[55]  K. Frick,et al.  Long-term continuous, but not daily, environmental enrichment reduces spatial memory decline in aged male mice , 2006, Neurobiology of Learning and Memory.

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

[57]  R. Muller,et al.  Multiple representations in the hippocampus , 1991, Hippocampus.

[58]  Edmund T. Rolls,et al.  The mechanisms for pattern completion and pattern separation in the hippocampus , 2013, Front. Syst. Neurosci..

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

[60]  M R Rosenzweig,et al.  Effects of differential experience on dendritic spine counts in rat cerebral cortex. , 1973, Journal of comparative and physiological psychology.

[61]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[62]  Bruce L. McNaughton,et al.  Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles , 1999, Nature Neuroscience.

[63]  J. Csicsvari,et al.  Organization of cell assemblies in the hippocampus , 2003, Nature.

[64]  Carol A Barnes,et al.  Experience-Dependent Coincident Expression of the Effector Immediate-Early Genes Arc and Homer 1a in Hippocampal and Neocortical Neuronal Networks , 2002, The Journal of Neuroscience.

[65]  W. Abraham,et al.  Enriched environment exposure alters the input-output dynamics of synaptic transmission in area CA1 of freely moving rats , 2005, Neuroscience Letters.

[66]  Kathryn J Jeffery,et al.  Heterogeneous Modulation of Place Cell Firing by Changes in Context , 2003, The Journal of Neuroscience.

[67]  J. O’Keefe,et al.  Rearing on Hind Legs, Environmental Novelty, and the Hippocampal Formation , 2006, Reviews in the neurosciences.

[68]  D. Bilkey,et al.  Excitotoxic lesions of the pre‐ and parasubiculum disrupt the place fields of hippocampal pyramidal cells , 2004, Hippocampus.

[69]  Nathalie L Rochefort,et al.  Sparsification of neuronal activity in the visual cortex at eye-opening , 2009, Proceedings of the National Academy of Sciences.

[70]  Sonja Grün,et al.  Cross-frequency interaction of the eye-movement related LFP signals in V1 of freely viewing monkeys , 2012, Front. Syst. Neurosci..

[71]  Michael M Merzenich,et al.  Lifelong plasticity in the rat auditory cortex: basic mechanisms and role of sensory experience. , 2011, Progress in brain research.

[72]  E. Argandoña,et al.  Enriched and Deprived Sensory Experience Induces Structural Changes and Rewires Connectivity during the Postnatal Development of the Brain , 2012, Neural plasticity.

[73]  P. Best,et al.  Place cells and silent cells in the hippocampus of freely-behaving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  D. Bilkey,et al.  Hippocampal place cells show increased sensitivity to changes in the local environment following prefrontal cortex lesions. , 2005, Cerebral cortex.

[75]  J. Banquet,et al.  Spatial Navigation and Hippocampal Place Cell Firing: The Problem of Goal Encoding , 2004, Reviews in the neurosciences.