DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A hypothesis for temporal coding of young and mature granule cells

Abstract

While it has been hypothesized that adult neurogenesis (NG) plays a role in the encoding of temporal information at long time-scales, the temporal relationship of immature cells to the highly rhythmic network activity of the hippocampus has been largely unexplored. Here, we present a theory for how the activity of immature adult-born granule cells relates to hippocampal oscillations. Our hypothesis is that theta rhythmic (5–10 Hz) excitatory and inhibitory inputs into the hippocampus could differentially affect young and mature granule cells due to differences in intrinsic physiology and synaptic inhibition between the two cell populations. Consequently, immature cell activity may occur at broader ranges of theta phase than the activity of their mature counterparts. We describe how this differential influence on young and mature granule cells could separate the activity of differently aged neurons in a temporal coding regime. Notably, this process could have considerable implications on how the downstream CA3 region interprets the information conveyed by young and mature granule cells. To begin to investigate the phasic behavior of granule cells, we analyzed in vivo recordings of the rat dentate gyrus (DG), observing that the temporal behavior of granule cells with respect to the theta rhythm is different betweenmore » rats with normal and impaired levels of NG. Specifically, in control animals, granule cells exhibit both strong and weak coupling to the phase of the theta rhythm. In contrast, the distribution of phase relationships in NG-impaired rats is shifted such that they are significantly stronger. These preliminary data support our hypothesis that immature neurons could distinctly affect the temporal dynamics of hippocampal encoding.« less

Authors:
 [1];  [1];  [1];  [2];  [3]
  1. University of California, San Diego, CA (United States)
  2. Salk Institute for Biological Studies, La Jolla, CA (United States)
  3. Sandia National Laboratory (SNL-NM), Albuquerque, NM (United States)
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); James S. McDonnell Foundation; National Science Foundation (NSF); USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1628202
Grant/Contract Number:  
NA0003525; SBE0542013; AC04-94AL85000.
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Neuroscience (Online)
Additional Journal Information:
Journal Name: Frontiers in Neuroscience (Online); Journal Volume: 7; Journal ID: ISSN 1662-453X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; adult neurogenesis; oscillations; dentate gyrus; hippocampus; temporal coding; granule cells

Citation Formats

Rangel, Lara M., Quinn, Laleh K., Chiba, Andrea A., Gage, Fred H., and Aimone, James B. A hypothesis for temporal coding of young and mature granule cells. United States: N. p., 2013. Web. doi:10.3389/fnins.2013.00075.
Rangel, Lara M., Quinn, Laleh K., Chiba, Andrea A., Gage, Fred H., & Aimone, James B. A hypothesis for temporal coding of young and mature granule cells. United States. https://doi.org/10.3389/fnins.2013.00075
Rangel, Lara M., Quinn, Laleh K., Chiba, Andrea A., Gage, Fred H., and Aimone, James B. Tue . "A hypothesis for temporal coding of young and mature granule cells". United States. https://doi.org/10.3389/fnins.2013.00075. https://www.osti.gov/servlets/purl/1628202.
@article{osti_1628202,
title = {A hypothesis for temporal coding of young and mature granule cells},
author = {Rangel, Lara M. and Quinn, Laleh K. and Chiba, Andrea A. and Gage, Fred H. and Aimone, James B.},
abstractNote = {While it has been hypothesized that adult neurogenesis (NG) plays a role in the encoding of temporal information at long time-scales, the temporal relationship of immature cells to the highly rhythmic network activity of the hippocampus has been largely unexplored. Here, we present a theory for how the activity of immature adult-born granule cells relates to hippocampal oscillations. Our hypothesis is that theta rhythmic (5–10 Hz) excitatory and inhibitory inputs into the hippocampus could differentially affect young and mature granule cells due to differences in intrinsic physiology and synaptic inhibition between the two cell populations. Consequently, immature cell activity may occur at broader ranges of theta phase than the activity of their mature counterparts. We describe how this differential influence on young and mature granule cells could separate the activity of differently aged neurons in a temporal coding regime. Notably, this process could have considerable implications on how the downstream CA3 region interprets the information conveyed by young and mature granule cells. To begin to investigate the phasic behavior of granule cells, we analyzed in vivo recordings of the rat dentate gyrus (DG), observing that the temporal behavior of granule cells with respect to the theta rhythm is different between rats with normal and impaired levels of NG. Specifically, in control animals, granule cells exhibit both strong and weak coupling to the phase of the theta rhythm. In contrast, the distribution of phase relationships in NG-impaired rats is shifted such that they are significantly stronger. These preliminary data support our hypothesis that immature neurons could distinctly affect the temporal dynamics of hippocampal encoding.},
doi = {10.3389/fnins.2013.00075},
journal = {Frontiers in Neuroscience (Online)},
number = ,
volume = 7,
place = {United States},
year = {Tue Jan 01 00:00:00 EST 2013},
month = {Tue Jan 01 00:00:00 EST 2013}
}

Works referenced in this record:

Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm
journal, January 2005


Hippocampal granule cells opt for early retirement
journal, August 2010

  • Alme, C. B.; Buzzetti, R. A.; Marrone, D. F.
  • Hippocampus, Vol. 20, Issue 10
  • DOI: 10.1002/hipo.20810

Minimal driving of hippocampal theta by the supramammillary nucleus during water maze learning
journal, June 2010

  • Ruan, Ming; Young, Calvin K.; McNaughton, Neil
  • Hippocampus, Vol. 21, Issue 10
  • DOI: 10.1002/hipo.20821

Put Them Out to Pasture? What Are Old Granule Cells Good for, Anyway…?
journal, September 2010

  • Aimone, James B.; Deng, Wei; Gage, Fred H.
  • Hippocampus, Vol. 20, Issue 10
  • DOI: 10.1002/hipo.20867

Phase relationship between hippocampal place units and the EEG theta rhythm
journal, July 1993


Selective Immunolesion of the Basal Forebrain Cholinergic Neurons: Effects on Hippocampal Activity During Sleep and Wakefulness in the Rat
journal, March 1995

  • Bassant, Marie H.; Apartis, Emmanuelle; Jazat-Poindessous, Frédérique R.
  • Neurodegeneration, Vol. 4, Issue 1
  • DOI: 10.1006/neur.1995.0007

Reversible inactivation of the medial septum: selective effects on the spontaneous unit activity of different hippocampal cell types
journal, October 1989


Hippocampal theta activity following selective lesion of the septal cholinergic systeM
journal, October 1994


Computational Influence of Adult Neurogenesis on Memory Encoding
journal, January 2009


Theta Oscillations Provide Temporal Windows for Local Circuit Computation in the Entorhinal-Hippocampal Loop
journal, October 2009


Neural Syntax: Cell Assemblies, Synapsembles, and Readers
journal, November 2010


Resolving New Memories: A Critical Look at the Dentate Gyrus, Adult Neurogenesis, and Pattern Separation
journal, May 2011


Pattern Separation: A Common Function for New Neurons in Hippocampus and Olfactory Bulb
journal, May 2011


Interneuron Diversity series: Containing the detonation – feedforward inhibition in the CA3 hippocampus
journal, November 2003


Theta Oscillations in the Hippocampus
journal, January 2002


Neuromodulation: acetylcholine and memory consolidation
journal, September 1999


Neurons born in the adult dentate gyrus form functional synapses with target cells
journal, July 2008

  • Toni, Nicolas; Laplagne, Diego A.; Zhao, Chunmei
  • Nature Neuroscience, Vol. 11, Issue 8
  • DOI: 10.1038/nn.2156

Optical controlling reveals time-dependent roles for adult-born dentate granule cells
journal, November 2012

  • Gu, Yan; Arruda-Carvalho, Maithe; Wang, Jia
  • Nature Neuroscience, Vol. 15, Issue 12
  • DOI: 10.1038/nn.3260

Synapse formation on neurons born in the adult hippocampus
journal, May 2007

  • Toni, Nicolas; Teng, E. Matthew; Bushong, Eric A.
  • Nature Neuroscience, Vol. 10, Issue 6
  • DOI: 10.1038/nn1908

Development of GABAergic inputs controls the contribution of maturing neurons to the adult hippocampal network
journal, February 2012

  • Li, Y.; Aimone, J. B.; Xu, X.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 11
  • DOI: 10.1073/pnas.1120754109

Chemotherapy disrupts learning, neurogenesis and theta activity in the adult brain
journal, October 2012

  • Nokia, Miriam S.; Anderson, Megan L.; Shors, Tracey J.
  • European Journal of Neuroscience, Vol. 36, Issue 11
  • DOI: 10.1111/ejn.12007

Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus
journal, February 2007


Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning
journal, April 2011

  • Brandon, Mark P.; Bogaard, Andrew R.; Libby, Christopher P.
  • Science, Vol. 332, Issue 6029
  • DOI: 10.1126/science.1201652

The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations
journal, April 2011


Theta Modulation in the Medial and the Lateral Entorhinal Cortices
journal, August 2010

  • Deshmukh, Sachin S.; Yoganarasimha, D.; Voicu, Horatiu
  • Journal of Neurophysiology, Vol. 104, Issue 2
  • DOI: 10.1152/jn.01141.2009

The Timing of Neuronal Development in Adult Hippocampal Neurogenesis
journal, December 2006

  • Piatti, Verónica C.; Espósito, M. Soledad; Schinder, Alejandro F.
  • The Neuroscientist, Vol. 12, Issue 6
  • DOI: 10.1177/1073858406293538

Reliable Activation of Immature Neurons in the Adult Hippocampus
journal, April 2009


Adult-Generated Hippocampal Neurons Allow the Flexible Use of Spatially Precise Learning Strategies
journal, May 2009


Spatial firing properties of hippocampal theta cells
journal, April 1990


Interdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis
journal, July 1999


Effects of acetylcholine on neuronal properties in entorhinal cortex
journal, January 2012

  • Heys, James G.; Schultheiss, Nathan W.; Shay, Christopher F.
  • Frontiers in Behavioral Neuroscience, Vol. 6
  • DOI: 10.3389/fnbeh.2012.00032

Works referencing / citing this record:

T2N as a new tool for robust electrophysiological modeling demonstrated for mature and adult-born dentate granule cells
journal, November 2017

  • Beining, Marcel; Mongiat, Lucas Alberto; Schwarzacher, Stephan Wolfgang
  • eLife, Vol. 6
  • DOI: 10.7554/elife.26517

Young adult born neurons enhance hippocampal dependent performance via influences on bilateral networks
journal, December 2016


Regulation and Function of Adult Neurogenesis: From Genes to Cognition
journal, October 2014


Low excitatory innervation balances high intrinsic excitability of immature dentate neurons
journal, April 2016

  • Dieni, Cristina V.; Panichi, Roberto; Aimone, James B.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11313

Exercising New Neurons to Vanquish Alzheimer Disease
journal, December 2018


Young adult born neurons enhance hippocampal dependent performance via influences on bilateral networks
journal, December 2016