Temporally selective contextual encoding in the dentate gyrus of the hippocampus

Rangel, L. M.; Alexander, A. S.; Aimone, J. B.; Wiles, J.; Gage, F. H.; Chiba, A. A.; Quinn, L. K.

doi:10.1038/ncomms4181

Temporally selective contextual encoding in the dentate gyrus of the hippocampus

Journal Article · Tue Feb 11 23:00:00 EST 2014 · Nature Communications

DOI:https://doi.org/10.1038/ncomms4181· OSTI ID:1623933

Rangel, L. M. ^[1]; Alexander, A. S. ^[2]; Aimone, J. B. ^[3]; Wiles, J. ^[4]; Gage, F. H. ^[5]; Chiba, A. A. ^[6]; Quinn, L. K. ^[2]

Univ. of California, San Diego, CA (United States). program in Neurosciences; Salk Institute for Biological Studies, La Jolla, CA (United States); DOE/OSTI
Univ. of California, San Diego, CA (United States). Dept. of Cognitive Science
Salk Institute for Biological Studies, La Jolla, CA (United States)
Univ. of Queensland, Brisbane, QLD (Australia). School of Information Technology and Electrical Engineering
Univ. of California, San Diego, CA (United States). program in Neurosciences; Salk Institute for Biological Studies, La Jolla, CA (United States)
Univ. of California, San Diego, CA (United States). program in Neurosciences; Univ. of California, San Diego, CA (United States). Dept. of Cognitive Science

A recent model of the hippocampus predicts that the unique properties of the dentate gyrus allow for temporal separation of events. This temporal separation is accomplished in part through the continual generation of new neurons, which, due to a transient window of hyperexcitability, could allow for preferential encoding of information present during their development. Here we obtain in vivo electrophysiological recordings and identify a cell population exhibiting activity that is selective to single contexts when rats experience a long temporal separation between context exposures during training. This selectivity is attenuated as the temporal separation between context exposures is shortened and is further attenuated when neurogenesis is reduced. Our data reveal the existence of a temporal orthogonalizing neuronal code within the dentate gyrus, a hallmark feature of episodic memory.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratories (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF)

Grant/Contract Number:: NA0003525

OSTI ID:: 1623933

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 5; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (36)

Hippocampal granule cells opt for early retirement Alme, C. B.; Buzzetti, R. A.; Marrone, D. F. Hippocampus, Vol. 20, Issue 10 https://doi.org/10.1002/hipo.20810	journal	August 2010
Spatial selectivity of unit activity in the hippocampal granular layer Jung, M. W.; McNaughton, B. L. Hippocampus, Vol. 3, Issue 2 https://doi.org/10.1002/hipo.450030209	journal	April 1993
Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input Markus, Etan J.; Barnes, Carol A.; McNaughton, Bruce L. Hippocampus, Vol. 4, Issue 4 https://doi.org/10.1002/hipo.450040404	journal	August 1994
Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats Thompson, L. T.; Best, P. J. Brain Research, Vol. 509, Issue 2 https://doi.org/10.1016/0006-8993(90)90555-p	journal	February 1990
Long-term memory for contextual attributes: Dissociation of amygdala and hippocampus Kesner, Raymond P.; Hardy, John D. Behavioural Brain Research, Vol. 8, Issue 2 https://doi.org/10.1016/0166-4328(83)90050-5	journal	May 1983
The temporal attributes of episodic memory Kesner, Raymond P.; Hunsaker, Michael R. Behavioural Brain Research, Vol. 215, Issue 2 https://doi.org/10.1016/j.bbr.2009.12.029	journal	December 2010
Computational Influence of Adult Neurogenesis on Memory Encoding Aimone, James B.; Wiles, Janet; Gage, Fred H. Neuron, Vol. 61, Issue 2 https://doi.org/10.1016/j.neuron.2008.11.026	journal	January 2009
Pattern Separation: A Common Function for New Neurons in Hippocampus and Olfactory Bulb Sahay, Amar; Wilson, Donald A.; Hen, René Neuron, Vol. 70, Issue 4 https://doi.org/10.1016/j.neuron.2011.05.012	journal	May 2011
Memory Time Shapiro, Matthew L. Neuron, Vol. 71, Issue 4 https://doi.org/10.1016/j.neuron.2011.08.006	journal	August 2011
The Human Hippocampus and Spatial and Episodic Memory Burgess, Neil; Maguire, Eleanor A.; O'Keefe, John Neuron, Vol. 35, Issue 4 https://doi.org/10.1016/s0896-6273(02)00830-9	journal	August 2002
Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. McClelland, James L.; McNaughton, Bruce L.; O'Reilly, Randall C. Psychological Review, Vol. 102, Issue 3 https://doi.org/10.1037/0033-295x.102.3.419	journal	July 1995
The interactions and dissociations of the dorsal hippocampus subregions: How the dentate gyrus, CA3, and CA1 process spatial information. Goodrich-Hunsaker, Naomi J.; Hunsaker, Michael R.; Kesner, Raymond P. Behavioral Neuroscience, Vol. 122, Issue 1 https://doi.org/10.1037/0735-7044.122.1.16	journal	January 2008
Potential role for adult neurogenesis in the encoding of time in new memories Aimone, James B.; Wiles, Janet; Gage, Fred H. Nature Neuroscience, Vol. 9, Issue 6 https://doi.org/10.1038/nn1707	journal	May 2006
Development of GABAergic inputs controls the contribution of maturing neurons to the adult hippocampal network Li, Y.; Aimone, J. B.; Xu, X. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1120754109	journal	February 2012
Chemotherapy disrupts learning, neurogenesis and theta activity in the adult brain Nokia, Miriam S.; Anderson, Megan L.; Shors, Tracey J. European Journal of Neuroscience, Vol. 36, Issue 11 https://doi.org/10.1111/ejn.12007	journal	October 2012
Mammalian Neural Stem Cells Gage, F. H. Science, Vol. 287, Issue 5457 https://doi.org/10.1126/science.287.5457.1433	journal	February 2000
Complementary Roles of Hippocampus and Medial Entorhinal Cortex in Episodic Memory Lipton, P. A.; Eichenbaum, H. Neural Plasticity, Vol. 2008 https://doi.org/10.1155/2008/258467	journal	January 2008
The Timing of Neuronal Development in Adult Hippocampal Neurogenesis Piatti, Verónica C.; Espósito, M. Soledad; Schinder, Alejandro F. The Neuroscientist, Vol. 12, Issue 6 https://doi.org/10.1177/1073858406293538	journal	December 2006
Adult-Generated Hippocampal Neurons Allow the Flexible Use of Spatially Precise Learning Strategies Garthe, Alexander; Behr, Joachim; Kempermann, Gerd PLoS ONE, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pone.0005464	journal	May 2009
Experience-Specific Functional Modification of the Dentate Gyrus through Adult Neurogenesis: A Critical Period during an Immature Stage Tashiro, A.; Makino, H.; Gage, F. H. Journal of Neuroscience, Vol. 27, Issue 12 https://doi.org/10.1523/jneurosci.4941-06.2007	journal	March 2007
Spatial Firing Correlates of Physiologically Distinct Cell Types of the Rat Dentate Gyrus Neunuebel, J. P.; Knierim, J. J. Journal of Neuroscience, Vol. 32, Issue 11 https://doi.org/10.1523/jneurosci.6038-11.2012	journal	March 2012
Neurogenesis in the dentate gyrus: carrying the message or dictating the tone Piatti, Verónica C.; Ewell, Laura A.; Leutgeb, Jill K. Frontiers in Neuroscience, Vol. 7 https://doi.org/10.3389/fnins.2013.00050	journal	January 2013
Modification of hippocampal circuitry by adult neurogenesis Song, Juan; M. Christian, Kimberly; Ming, Guo-li Developmental Neurobiology, Vol. 72, Issue 7 https://doi.org/10.1002/dneu.22014	journal	June 2012
Neurogenesis may relate to some but not all types of hippocampal-dependent learning Shors, Tracey J.; Townsend, David A.; Zhao, Mingrui Hippocampus, Vol. 12, Issue 5 https://doi.org/10.1002/hipo.10103	journal	January 2002
Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats Thompson, L. T.; Best, P. J. Brain Research, Vol. 509, Issue 2 https://doi.org/10.1016/0006-8993(90)90555-P	journal	February 1990
The Human Hippocampus and Spatial and Episodic Memory Burgess, Neil; Maguire, Eleanor A.; O'Keefe, John Neuron, Vol. 35, Issue 4 https://doi.org/10.1016/S0896-6273(02)00830-9	journal	August 2002
A Critical Period for Enhanced Synaptic Plasticity in Newly Generated Neurons of the Adult Brain Ge, Shaoyu; Yang, Chih-hao; Hsu, Kuei-sen Neuron, Vol. 54, Issue 4 https://doi.org/10.1016/j.neuron.2007.05.002	journal	May 2007
Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events MacDonald, Christopher J.; Lepage, Kyle Q.; Eden, Uri T. Neuron, Vol. 71, Issue 4 https://doi.org/10.1016/j.neuron.2011.07.012	journal	August 2011
Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. McClelland, James L.; McNaughton, Bruce L.; O'Reilly, Randall C. Psychological Review, Vol. 102, Issue 3 https://doi.org/10.1037/0033-295X.102.3.419	journal	July 1995
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Squire, Larry R. Psychological Review, Vol. 99, Issue 2 https://doi.org/10.1037/0033-295X.99.2.195	journal	January 1992
Simple Memory: A Theory for Archicortex Marr, D. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 262, Issue 841 https://doi.org/10.1098/rstb.1971.0078	journal	July 1971
Neurogenesis and the spacing effect: Learning over time enhances memory and the survival of new neurons Sisti, H. M.; Glass, A. L.; Shors, T. J. Learning & Memory, Vol. 14, Issue 5 https://doi.org/10.1101/lm.488707	journal	May 2007
Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus Leutgeb, J. K.; Leutgeb, S.; Moser, M. -B. Science, Vol. 315, Issue 5814 https://doi.org/10.1126/science.1135801	journal	February 2007
Unique Processing During a Period of High Excitation/Inhibition Balance in Adult-Born Neurons Marín-Burgin, Antonia; Mongiat, Lucas A.; Pardi, M. Belén Science, Vol. 335, Issue 6073 https://doi.org/10.1126/science.1214956	journal	January 2012
Experience-Specific Functional Modification of the Dentate Gyrus through Adult Neurogenesis: A Critical Period during an Immature Stage Tashiro, A.; Makino, H.; Gage, F. H. Journal of Neuroscience, Vol. 27, Issue 12 https://doi.org/10.1523/JNEUROSCI.4941-06.2007	journal	March 2007
Spatial Firing Correlates of Physiologically Distinct Cell Types of the Rat Dentate Gyrus Neunuebel, J. P.; Knierim, J. J. Journal of Neuroscience, Vol. 32, Issue 11 https://doi.org/10.1523/JNEUROSCI.6038-11.2012	journal	March 2012

Cited By (23)

Transcending time in the brain: How event memories are constructed from experience Clewett, David; DuBrow, Sarah; Davachi, Lila Hippocampus, Vol. 29, Issue 3 https://doi.org/10.1002/hipo.23074	journal	February 2019
A shared representation of order between encoding and recognition in visual short-term memory Kalm, Kristjan; Norris, Dennis NeuroImage, Vol. 155 https://doi.org/10.1016/j.neuroimage.2017.04.047	journal	July 2017
Adult Neurogenesis and the Future of the Rejuvenating Brain Circuits Lepousez, Gabriel; Nissant, Antoine; Lledo, Pierre-Marie Neuron, Vol. 86, Issue 2 https://doi.org/10.1016/j.neuron.2015.01.002	journal	April 2015
Low excitatory innervation balances high intrinsic excitability of immature dentate neurons Dieni, Cristina V.; Panichi, Roberto; Aimone, James B. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11313	journal	April 2016
Attenuated Late-PhaseArcTranscription in the Dentate Gyrus of Mice LackingEgr3 Maple, Amanda; Lackie, Rachel E.; Elizalde, Diana I. Neural Plasticity, Vol. 2017 https://doi.org/10.1155/2017/6063048	journal	January 2017
Modeling of Brain-Like Concept Coding with Adulthood Neurogenesis in the Dentate Gyrus Wang, Ye; Gao, Yan; Deng, Yaling Computational Intelligence and Neuroscience, Vol. 2019 https://doi.org/10.1155/2019/2367075	journal	November 2019
Adult hippocampal neurogenesis poststroke: More new granule cells but aberrant morphology and impaired spatial memory Woitke, Florus; Ceanga, Mihai; Rudolph, Max PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0183463	journal	September 2017
Reading positional codes with fMRI: Problems and solutions. Kalm, Kristjan; Norris, Dennis PLOS https://doi.org/10.17863/cam.21323	journalarticle	January 2017
Neuroactive Steroids Reverse Tonic Inhibitory Deficits in Fragile X Syndrome Mouse Model Modgil, Amit; Vien, Thuy N.; Ackley, Michael A. Frontiers in Molecular Neuroscience, Vol. 12 https://doi.org/10.3389/fnmol.2019.00015	journal	February 2019
Theta and beta oscillatory dynamics in the dentate gyrus reveal a shift in network processing state during cue encounters Rangel, Lara M.; Chiba, Andrea A.; Quinn, Laleh K. Frontiers in Systems Neuroscience, Vol. 9 https://doi.org/10.3389/fnsys.2015.00096	journal	July 2015
Age-related changes in dentate gyrus cell numbers, neurogenesis, and associations with cognitive impairments in the rhesus monkey Ngwenya, Laura B.; Heyworth, Nadine C.; Shwe, Yamin Frontiers in Systems Neuroscience, Vol. 9 https://doi.org/10.3389/fnsys.2015.00102	journal	July 2015
Correction: The computational nature of memory modification Gershman, Samuel J.; Monfils, Marie-H; Norman, Kenneth A. eLife, Vol. 6 https://doi.org/10.7554/elife.28693	journal	May 2017
Image-guided cranial irradiation-induced ablation of dentate gyrus neurogenesis impairs extinction of recent morphine reward memories Rivera, Phillip D.; Simmons, Steven J.; Reynolds, Ryan P. Hippocampus, Vol. 29, Issue 8 https://doi.org/10.1002/hipo.23071	journal	February 2019
Adult-born dentate granule cell excitability depends on the interaction of neuron age, ontogenetic age and experience Ohline, S. M.; Wake, K. L.; Hawkridge, M. -V. Brain Structure and Function, Vol. 223, Issue 7 https://doi.org/10.1007/s00429-018-1685-2	journal	May 2018
Adult hippocampal neurogenesis and cognitive flexibility — linking memory and mood Anacker, Christoph; Hen, René Nature Reviews Neuroscience, Vol. 18, Issue 6 https://doi.org/10.1038/nrn.2017.45	journal	May 2017
Time cells in the hippocampus: a new dimension for mapping memories Eichenbaum, Howard Nature Reviews Neuroscience, Vol. 15, Issue 11 https://doi.org/10.1038/nrn3827	journal	October 2014
Functions of adult-born neurons in hippocampal memory interference and indexing Miller, Samara M.; Sahay, Amar Nature Neuroscience, Vol. 22, Issue 10 https://doi.org/10.1038/s41593-019-0484-2	journal	September 2019
The Computational Nature of Memory Modification Gershman, Samuel J.; Monfils, Marie-H; Norman, Kenneth A. eLife https://doi.org/10.1101/036442	journal	September 2016
Adult Hippocampal Neurogenesis in Parkinson’s Disease: Impact on Neuronal Survival and Plasticity Regensburger, Martin; Prots, Iryna; Winner, Beate Neural Plasticity, Vol. 2014 https://doi.org/10.1155/2014/454696	journal	January 2014
Adult Hippocampal Neurogenesis: Regulation and Possible Functional and Clinical Correlates Baptista, Pedro; Andrade, José P. Frontiers in Neuroanatomy, Vol. 12 https://doi.org/10.3389/fnana.2018.00044	journal	June 2018
Modeling Contextual Modulation of Memory Associations in the Hippocampus Pilly, Praveen K.; Howard, Michael D.; Bhattacharyya, Rajan Frontiers in Human Neuroscience, Vol. 12 https://doi.org/10.3389/fnhum.2018.00442	journal	November 2018
Young adult born neurons enhance hippocampal dependent performance via influences on bilateral networks Zhuo, Jia-Min; Tseng, Hua-an; Desai, Mitul eLife, Vol. 5 https://doi.org/10.7554/elife.22429	journal	December 2016
The computational nature of memory modification Gershman, Samuel J.; Monfils, Marie-H; Norman, Kenneth A. eLife, Vol. 6 https://doi.org/10.7554/elife.23763	journal	March 2017

Similar Records

Disrupting nNOS-PSD-95 coupling in the hippocampal dentate gyrus promotes extinction memory retrieval

Journal Article · Sat Nov 04 00:00:00 EDT 2017 · Biochemical and Biophysical Research Communications · OSTI ID:22719135

Early effects of trimethyltin on the dentate gyrus basket cells: a morphological study

Journal Article · Mon Dec 31 23:00:00 EST 1984 · J. Toxicol. Environ. Health; (United States) · OSTI ID:5801624

Dopaminergic inputs in the dentate gyrus direct the choice of memory encoding

Journal Article · Tue Sep 13 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1328121

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics

Temporally selective contextual encoding in the dentate gyrus of the hippocampus

Citation Formats

References (36)

Cited By (23)

Similar Records

Related Subjects