Role for short term plasticity and OLM cells in containing spread of excitation (Hummos et al 2014)

 Download zip file   Auto-launch 
Help downloading and running models
Accession:168314
This hippocampus model was developed by matching experimental data, including neuronal behavior, synaptic current dynamics, network spatial connectivity patterns, and short-term synaptic plasticity. Furthermore, it was constrained to perform pattern completion and separation under the effects of acetylcholine. The model was then used to investigate the role of short-term synaptic depression at the recurrent synapses in CA3, and inhibition by basket cell (BC) interneurons and oriens lacunosum-moleculare (OLM) interneurons in containing the unstable spread of excitatory activity in the network.
Reference:
1 . Hummos A, Franklin CC, Nair SS (2014) Intrinsic mechanisms stabilize encoding and retrieval circuits differentially in a hippocampal network model. Hippocampus 24:1430-1448 [PubMed]
Model Information (Click on a link to find other models with that property)
Model Type: Realistic Network;
Brain Region(s)/Organism: Hippocampus;
Cell Type(s): Dentate gyrus granule cell; Hippocampus CA3 pyramidal cell; Hippocampus CA3 basket cell; Hippocampus CA3 stratum oriens lacunosum-moleculare interneuron; Abstract Izhikevich neuron;
Channel(s):
Gap Junctions:
Receptor(s):
Gene(s):
Transmitter(s): Acetylcholine; Gaba; Glutamate;
Simulation Environment: NEURON;
Model Concept(s): Activity Patterns; Epilepsy; Storage/recall;
Implementer(s):
Search NeuronDB for information about:  Dentate gyrus granule cell; Hippocampus CA3 pyramidal cell; Hippocampus CA3 basket cell; Acetylcholine; Gaba; Glutamate;
This is the readme for the model associated with the paper:

Hummos A, Franklin CC, Nair SS (2014) Intrinsic mechanisms stabilize
encoding and retrieval circuits differentially in a hippocampal
network model. Hippocampus

This model was contributed by Ali Hummos.

A biologically realistic model of the hippocampus matched closely
using parameters from published literature. The model is constrained
to perform pattern separation and completion and is used to examine
the unbounded spread of excitation during these processes.

This model has been developed using the NEURON simulator (Hines and
Carnavale, 2008).

Summary of files: 

- Hipp.hoc:             Main file to run the simulations and adjust parameters
- Protocol. hoc:        Triggers changes in ACH levels and synaptic
                        plasticity
- Connect.hoc:		Creates synaptic connections
- StimuliPatterns.hoc:  Creates the input patterns for the encoding
                        and retrieval experiment
- StimuliStability.hoc: Creates the input patterns for the network
                        stability profile experiment
-MakeLocations.hoc:     Creates three dimensional locations for
                        modeled neurons
- Izh.mod:              Defines the Izhikevich cell model as a
                        mechanism attached to biophysical cells
- Templates.hoc:        Defines all the cell types and their
                        parameters
- pyr2pyr.mod:          Defines the synapse object for excitatory
                        synapses
- Inter2pyr.mod:        Defines the synapse object for inhibitory
                        synapses
- Synapses.txt:         A Comma separated table containing all
                        parameters necessary to define synaptic
                        connections between cell populations

Usage:

- The file Hipp.hoc can be used to run the simulation, but prior to
  that the experiment parameters must be set up by changing a few
  variables as follows.

1) OutPath: Specifies the folder path where the output files from the
simulation will be stored.  No graphs are produced by the Neuron code
but rather output is stored in data files.
2) expSig: a unique identifier for each experiment as specified by the
user.  This identifier is added to names of the files produced by the
simulation, to allow these files to be accurately identified in the
analysis stage.
3) Experiment: the value of the variable Experiment determines the
pattern of inputs to EC neurons, the duration of the experiment,
activation of long-term plasticity, and changes in the level of
neuromodulators.  All these experiment parameters are set up in the
file protocol.hoc based on the value of the variable Experiment.  The
available experimental protocols are as follows:

Experiment = 0          this is the experiment presented in the
methods section of the paper, where all patterns 1 (consists of 10
randomly selected EC neurons) is presented to the network for encoding
for five trials, with LTP activated, and ACh set to high.  Followed by
the presentation of patterns 1 through 11 with LTP inactivated and ACh
set to the value assigned to the variable "Mods2".  The value of this
variable can be set by editing the file Hipp.hoc and it controls the
level of ACh during retrieval, to examine the effects of the
neuromodulator on the dynamics of retrieval.

Experiment = 2          this is a modified protocol where the network
learns both pattern 1 and pattern 11 interleaved in 10 trials.  Then
retrieval is tested with the probe patterns that gradually morph from
pattern 1 to pattern 11.  The results produced were similar To
Experiment=0 and were not reported in the paper.

Experiment = 3          this is the main experiment from the paper examining
network stability.  An increasing number of EC neurons receive a
stimulus of one action potential every 500 ms.  ACh is constant in
this experiment and is set to the value assigned to the variable
Mods2.

Experiment = 4          this is a short experiment where 20 EC neurons
receive an action potential at times zero and the response of CA3
pyramidal cells and well and inhibition are monitored (See figure
10D).

4) ACHlevel: this variable determines the level of the neuromodulator
Acetylcholine during the experiment.  For experiment 3, and it
determines the level of the neuromodulator for the whole experiment,
whereas for experiment 0, it only determines the level during the
retrieval phase.

5) Seed: the value from this variable is used to seed the
randomization process, thereby each value would produce a different
random version of the network with different connectivity and initial
states.  Currently, the code is set to read this value from a text
file "seed.txt".  A batch file is included with the code to help
run each experiment for 10 different seeds.  After updating the folder
paths in the batch file, or it can be used to run the experiment for
each value in the file "/inputs/seeds.txt".

6) Network connectivity: the connectivity of the network can be
controlled by editing the relevant section in the file connect.hoc.
This section of code copied below, specifies which neuronal
populations are to be connected.  Connections between any two cell
populations can be removed simply by commenting out the relevant line
(in neuron this is done by adding //at the beginning of the line).

ConnectAreas(EC, CA3e, EC2CA3e, Excitatory)
ConnectAreas(EC, CA3b, EC2CA3b, Excitatory)

ConnectAreas(DGg, CA3b, DGg2CA3b, Excitatory) 

ConnectAreas(CA3e, CA3e, CA3e2CA3e, Excitatory) 
ConnectAreas(CA3e, CA3b, CA3e2CA3b, Excitatory) 

// ConnectAreas(CA3o, CA3e, CA3o2CA3e, Inhibitory)
// ConnectAreas(CA3b, CA3e, CA3b2CA3e, Inhibitory)

// ConnectAreas(CA3b, CA3o, CA3b2CA3o, Inhibitory)

ConnectMF = 1

ConnectAreas(EC, DGg, EC2DGg, Excitatory)
ConnectAreas(EC, DGb, EC2DGb, Excitatory)

ConnectAreas(DGg, DGb, DGg2DGb, Excitatory)

ConnectAreas(DGh, DGg, DGh2DGg, Inhibitory)
ConnectAreas(DGb, DGg, DGb2DGg, Inhibitory)

ConnectAreas(DGb, DGh, DGb2DGh, Inhibitory)

(note that in this example above CA3 OLM (CA3o) and BC (CA3b)
interneurons are disconnected from pyramidal cells)

7) Output files: by default, the simulator produces files with a
record of all the spike times and all areas in the model.  In
addition, it can also produce files containing all the synaptic
current values, synaptic weight values, and neuronal membrane
potentials.  The additional output files can be produced by assigning
a value of 1 to a subset of three variables in the WriteOutput.hoc
file.
The simulator by default outputs spike times for each cell
population. It creates text files with the following naming rule:
OutPath + IDstring + "Spiketimes" + Area code + .txt
IDstring = Acetylcholine level + Experiment + Seed + expSig
The string Spiketimes is constant and is used to denote these files as
containing spike times.  Seed is the value used to initialize the
random process.
Area code, denotes which cell population the spike times come
from. Modeled areas has the following area codes:

EC: 0	
CA3 pyr: 1	OLM: 2		BC: 3		
DG GC: 4	HIPP: 5		BC: 6

Similarly, the simulator can also create output files for membrane
potentials, synaptic currents, and synaptic weights as they change
across the simulation. File naming for membrane potentials is as
described above for spike times except that the string "spiketimes" is
replaced by "volts". For synaptic currents and synaptic weights one
file is generated for each. The file contains a comma separated table
with the first column containing the simulation time values, and
subsequent columns each representing the current or the weight value
of a synapse as it changes over time. The first row in each of these
columns contains the synapse ID number. This ID number can be
referenced against another table in the file called connections.txt
which has the presynaptic neuron ID and area code and the postsynaptic
neuron ID and area code as well.

These files are produced in the "writetoutput.hoc" file. If the files
for the membrane potentials, synaptic currents, and or weights are
needed as output from the simulation, the code to produce them can be
activated by setting the variables Writesvolts, Writecurrents, and/or
Writeweights to a value of 1.

Matlab analysis:

The data files generated by the Neuron simulator are further analyzed
in MATLAB. We here provide a brief description of the Matlab scripts
included.

function [profiles] = Stability(fileSearch, path)

Stability.m: This script analyzes the stability profile of the network
given the Spiketimes of the neurons.  The script defines a function
that is used as follows:

Inputs:

- File searches: A cell array of 1 to 3 strings that are used to
  identify 1 to 3 sets of experiment files.  This algorithm uses the
  naming rule of output files employed by the neuron code.  The
  strings can use wildcard searches to capture all the files that need
  to

- be included in the analysis.  See below for an example.

- OutputPath: a string containing the relative path where the output
  files can be found.

Example:

- Stability({'139full', '13*OLMoff'},'.\Outputs\') 

Output files for these examples are included with the code.
Note that the second file search string uses a star instead of seed
number to capture all files for this experiment which was run with
multiple different seeds.
  
Correlation.m: Imports results from the pattern completion than
separation experiment and calculates correlation between outputs
generated by patterns 1 to 11 and the output generated by pattern 1.
function [corrs] = Correlation (FileSearch, OutPath)
Inputs:
- FileSearch: A string that uniquely identifies a set of experiments.
  This algorithm uses the naming rule of output files employed by the
  neuron code.  The string can use wildcard searches to capture all
  the files that need to be included in the analysis.  See below for
  an example.
- OutPath: A string containing the relative path where the output
  files can be found.
Example:
- Correlation('00*seps', '.\Outputs\') 
- Example output files are included.

For assistance are any questions, please contact:
       Ali Hummos, MD
hummosa@gmail.com
Health Informatics, University of Missouri Columbia


Hummos A, Franklin CC, Nair SS (2014) Intrinsic mechanisms stabilize encoding and retrieval circuits differentially in a hippocampal network model. Hippocampus 24:1430-1448[PubMed]

References and models cited by this paper

References and models that cite this paper

Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3 Suppl:1178-83 [PubMed]

Acsady L, Kamondi A, Sik A, Freund T, Buzsaki G (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18:3386-403 [PubMed]

Ali AB, Deuchars J, Pawelzik H, Thomson AM (1998) CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J Physiol 507 ( Pt 1):201-17 [PubMed]

Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol 507 ( Pt 1):185-99 [PubMed]

Bakker A, Kirwan CB, Miller M, Stark CE (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640-2 [PubMed]

Barkai E, Bergman RE, Horwitz G, Hasselmo ME (1994) Modulation of associative memory function in a biophysical simulation of rat piriform cortex. J Neurophysiol 72:659-77 [Journal] [PubMed]

Barry C, Heys JG, Hasselmo ME (2012) Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells. Front Neural Circuits 6:5-2 [PubMed]

Bartos M, Sauer J-F, Vida I, Kulik A (2010) Fast and slow GABAergic transmission in hippocampal circuits Hippocampal Microcircuits, Cutsuridis V:Graham B:Cobb S:Vida I, ed. pp.129

Baude A, Bleasdale C, Dalezios Y, Somogyi P, Klausberger T (2007) Immunoreactivity for the GABAA receptor alpha1 subunit, somatostatin and Connexin36 distinguishes axoaxonic, basket, and bistratified interneurons of the rat hippocampus. Cereb Cortex 17:2094-107 [PubMed]

Beyeler A, Retailleau A, Molter C, Mehidi A, Szabadics J, Leinekugel X (2013) Recruitment of Perisomatic Inhibition during Spontaneous Hippocampal Activity In Vitro. PLoS One 8:e66509-107 [PubMed]

Bianchi R, Wong RK (1994) Carbachol-induced synchronized rhythmic bursts in CA3 neurons of guinea pig hippocampus in vitro. J Neurophysiol 72:131-8 [PubMed]

Bliss TV, Collinridge G, Morris RG (2007) Synaptic plasticity in the hippocampus The Hippocampus book, Andersen P:Morris RG:Amaral DG:Bliss TV:O`Keefe J, ed. pp.343

Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-56 [PubMed]

Bower MR, Buckmaster PS (2008) Changes in granule cell firing rates precede locally recorded spontaneous seizures by minutes in an animal model of temporal lobe epilepsy. J Neurophysiol 99:2431-42 [PubMed]

Brown JT, Randall AD (2009) Activity-dependent depression of the spike after-depolarization generates long-lasting intrinsic plasticity in hippocampal CA3 pyramidal neurons. J Physiol 587:1265-81 [PubMed]

Buhl E, Whittington M (2007) Local circuits The Hippocampus Book, Andersen P:Morris RGM:Amaral DG:Bliss TVP:O`Keefe J, ed. pp.297

Buhl EH, Szilagyi T, Halasy K, Somogyi P (1996) Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus in vitro. Hippocampus 6:294-305 [PubMed]

Carnevale NT, Hines ML (2006) The NEURON Book

Cea-del Rio CA, Lawrence JJ, Tricoire L, Erdelyi F, Szabo G, McBain CJ (2010) M3 muscarinic acetylcholine receptor expression confers differential cholinergic modulation to neurochemically distinct hippocampal basket cell subtypes. J Neurosci 30:6011-24 [PubMed]

Cobb S, Lawrence JJ (2010) Neuromodulation of hippocampal cells and circuits Hippocampal Microcircuits, Cutsuridis V:Graham B:Cobb S:Vida I, ed. pp.187

Cossart R, Bernard C, Ben-Ari Y (2005) Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 28:108-15 [PubMed]

Cutsuridis V, Cobb S, Graham BP (2009) Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 20(3):423-46 [Journal] [PubMed]

   Encoding and retrieval in a model of the hippocampal CA1 microcircuit (Cutsuridis et al. 2009) [Model]

Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission Methods In Neuronal Modeling, Koch C:Segev I, ed. pp.1

   Kinetic synaptic models applicable to building networks (Destexhe et al 1998) [Model]

Do VH, Martinez CO, Martinez JL, Derrick BE (2002) Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo. J Neurophysiol 87:669-78 [PubMed]

Doucette TA, Bernard PB, Husum H, Perry MA, Ryan CL, Tasker RA (2004) Low doses of domoic acid during postnatal development produce permanent changes in rat behaviour and hippocampal morphology. Neurotox Res 6:555-63 [PubMed]

Gaiarsa JL, Caillard O, Ben-Ari Y (2002) Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25:564-70 [PubMed]

Geiger JR, Lubke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009-23 [PubMed]

   Fast AMPA receptor signaling (Geiger et al 1997) [Model]

Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-7 [PubMed]

Hasselmo ME, Bodelon C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793-817 [PubMed]

Hasselmo ME, Fehlau BP (2001) Differences in time course of ACh and GABA modulation of excitatory synaptic potentials in slices of rat hippocampus. J Neurophysiol 86:1792-802 [PubMed]

Hasselmo ME, Schnell E, Barkai E (1995) Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15:5249-62 [Journal] [PubMed]

   Fixed point attractor (Hasselmo et al 1995) [Model]

Hasselmo ME, Wyble BP (1997) Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav Brain Res 89:1-34 [PubMed]

Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319-28 [PubMed]

Henze DA, Wittner L, Buzsaki G (2002) Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5:790-5 [PubMed]

Hoskison MM, Connor JA, Shuttleworth CW (2004) GABA(B)-receptor modulation of short-term synaptic depression at an excitatory input to murine hippocampal CA3 pyramidal neurons. Neurosci Lett 365:48-53 [PubMed]

Hosseini-Sharifabad M, Nyengaard JR (2007) Design-based estimation of neuronal number and individual neuronal volume in the rat hippocampus. J Neurosci Methods 162:206-14 [PubMed]

Hunsaker MR, Kesner RP (2013) The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neurosci Biobehav Rev 37:36-58 [PubMed]

Ikonen S, McMahan R, Gallagher M, Eichenbaum H, Tanila H (2002) Cholinergic system regulation of spatial representation by the hippocampus. Hippocampus 12:386-97 [PubMed]

Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569-72 [Journal] [PubMed]

   Artificial neuron model (Izhikevich 2003, 2004, 2007) [Model]

Izhikevich EM (2007) Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting [Journal]

   Artificial neuron model (Izhikevich 2003, 2004, 2007) [Model]

Katona I, Acsady L, Freund TF (1999) Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88:37-55 [PubMed]

Kim D, Pare D, Nair SS (2013) Assignment of model amygdala neurons to the fear memory trace depends on competitive synaptic interactions. J Neurosci 33:14354-8 [PubMed]

Kim D, Pare D, Nair SS (2013) Mechanisms contributing to the induction and storage of Pavlovian fear memories in the lateral amygdala. Learn Mem 20:421-30 [Journal] [PubMed]

   A 1000 cell network model for Lateral Amygdala (Kim et al. 2013) [Model]

Kitajima T, Hara KI (1997) An integrated model for activity-dependent synaptic modifications Neural Netw 10:413-421

Kosaka T, Katsumaru H, Hama K, Wu JY, Heizmann CW (1987) GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-30 [PubMed]

Kremin T, Hasselmo ME (2007) Cholinergic suppression of glutamatergic synaptic transmission in hippocampal region CA3 exhibits laminar selectivity: Implication for hippocampal network dynamics. Neuroscience 149:760-7 [PubMed]

Kunec S, Hasselmo ME, Kopell N (2005) Encoding and retrieval in the CA3 region of the hippocampus: a model of theta-phase separation. J Neurophysiol 94:70-82 [PubMed]

Lawrence JJ, McBain CJ (2003) Interneuron diversity series: containing the detonation--feedforward inhibition in the CA3 hippocampus. Trends Neurosci 26:631-40 [PubMed]

Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006) Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 570:595-610 [PubMed]

Lee I, Kesner RP (2004) Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14:66-76 [PubMed]

Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-6 [PubMed]

Li G, Nair SS, Quirk GJ (2009) A biologically realistic network model of acquisition and extinction of conditioned fear associations in lateral amygdala neurons. J Neurophysiol 101:1629-46 [PubMed]

Ludwig A, Uvarov P, Pellegrino C, Thomas-Crusells J, Schuchmann S, Saarma M, Airaksinen MS, R (2011) Neurturin evokes MAPK-dependent upregulation of Egr4 and KCC2 in developing neurons. Neural Plast 2011:1-8 [PubMed]

Maccaferri G (2005) Stratum oriens horizontal interneurone diversity and hippocampal network dynamics. J Physiol 562:73-80 [PubMed]

Martin CB, Mirsattari SM, Pruessner JC, Pietrantonio S, Burneo JG, Hayman-Abello B, Köhler S (2012) Dejà vu in unilateral temporal-lobe epilepsy is associated with selective familiarity impairments on experimental tasks of recognition memory. Neuropsychologia 50:2981-91 [PubMed]

McClelland JL, Goddard NH (1996) Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus 6:654-65 [PubMed]

McMahon DB, Barrionuevo G (2002) Short- and long-term plasticity of the perforant path synapse in hippocampal area CA3. J Neurophysiol 88:528-33 [PubMed]

McQuiston AR, Madison DV (1999) Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J Neurosci 19:5693-702 [PubMed]

McQuiston AR, Madison DV (1999) Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19:2887-96 [PubMed]

Meeter M, Murre JM, Talamini LM (2004) Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits. Hippocampus 14:722-41 [PubMed]

Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol 428:61-77 [PubMed]

Miles R, Wong RK (1986) Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J Physiol 373:397-418 [PubMed]

Miles R, Wong RK (1987) Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 388:611-29 [PubMed]

Miles R, Wong RK (2007) Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306:371-3 [PubMed]

Misgeld U, Muller W, Polder HR (1989) Potentiation and suppression by eserine of muscarinic synaptic transmission in the guinea-pig hippocampal slice. J Physiol 409:191-206 [PubMed]

Mizuseki K, Royer S, Diba K, Buzsaki G (2012) Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons. Hippocampus 22:1659-80 [PubMed]

Naber PA, Caballero-Bleda M, Jorritsma-Byham B, Witter MP (1997) Parallel input to the hippocampal memory system through peri- and postrhinal cortices. Neuroreport 8:2617-21 [PubMed]

Neunuebel JP, Knierim JJ (2014) CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation. Neuron 81:416-27 [PubMed]

Newman EL, Gupta K, Climer JR, Monaghan CK, Hasselmo ME (2012) Cholinergic modulation of cognitive processing: insights drawn from computational models. Front Behav Neurosci 6:24-27 [PubMed]

Nolan CR, Wyeth G, Milford M, Wiles J (2011) The race to learn: spike timing and STDP can coordinate learning and recall in CA3. Hippocampus 21:647-60 [PubMed]

O'Reilly RC, McClelland JL (1994) Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4:661-82 [PubMed]

Perry MA, Ryan CL, Tasker RA (2009) Effects of low dose neonatal domoic acid administration on behavioural and physiological response to mild stress in adult rats. Physiol Behav 98:53-9 [PubMed]

Rogers JL, Kesner RP (2003) Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol Learn Mem 80:332-42 [PubMed]

Rogers JL, Kesner RP (2013) Cholinergic modulation of the hippocampus during encoding and retrieval of tone-shock-induced fear conditioning. Learn Mem 11:102-7 [PubMed]

Rolls ET, Kesner RP (2006) A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79:1-48 [PubMed]

Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsaki G (2012) Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15:769-75 [PubMed]

Seress L, Pokorny J (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J Anat 133:181-95 [PubMed]

Shouval HZ, Bear MF, Cooper LN (2002) A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc Natl Acad Sci U S A 99:10831-6 [PubMed]

Sik A, Penttonen M, Ylinen A, Buzsaki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651-65 [PubMed]

Staley KJ, Otis TS, Mody I (1992) Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J Neurophysiol 67:1346-58 [Journal] [PubMed]

Sussillo D, Toyoizumi T, Maass W (2007) Self-tuning of neural circuits through short-term synaptic plasticity. J Neurophysiol 97:4079-95 [PubMed]

Szabadics J, Soltesz I (2009) Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J Neurosci 29:4239-51 [PubMed]

Toth K (2010) Glutamatergic neurotransmission in the hippocampus Hippocampal Microcircuits, Cutsuridis V:Graham B:Cobb S:Vida I, ed. pp.99

Toth K, Suares G, Lawrence JJ, Philips-Tansey E, McBain CJ (2000) Differential mechanisms of transmission at three types of mossy fiber synapse. J Neurosci 20:8279-89 [PubMed]

Traub RD, Miles R, Wong RK (1987) Models of synchronized hippocampal bursts in the presence of inhibition. I. Single population events. J Neurophysiol 58:739-51 [Journal] [PubMed]

Treves A, Rolls ET (1992) Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2:189-99 [PubMed]

Varela JA, Sen K, Gibson J, Fost J, Abbott LF, Nelson SB (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17:7926-40 [Journal] [PubMed]

   Short term plasticity of synapses onto V1 layer 2/3 pyramidal neuron (Varela et al 1997) [Model]

Vida I (2010) Morphology of hippocampal neurons Hippocampal Microcircuits, Cutsuridis V:Graham B:Cobb S:Vida I, ed. pp.27

Vogt KE, Regehr WG (2001) Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21:75-83 [PubMed]

Witter MP (2010) Connectivity of the hippocampus Hippocampal Microcircuits, Cutsuridis V:Graham B:Cobb S:Vida I, ed. pp.5

Wittner L, Henze DA, Zaborszky L, Buzsaki G (2006) Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons. Eur J Neurosci 24:1286-98 [PubMed]

Wittner L, Henze DA, Zaborszky L, Buzsaki G (2007) Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct Funct 212:75-83 [PubMed]

   [18 reconstructed morphologies on NeuroMorpho.Org]

Woodin MA, Ganguly K, Poo MM (2003) Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39:807-20 [PubMed]

Woolf NJ (1991) Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475-524 [PubMed]

Wyeth MS, Zhang N, Mody I, Houser CR (2010) Selective reduction of cholecystokinin-positive basket cell innervation in a model of temporal lobe epilepsy. J Neurosci 30:8993-9006 [PubMed]

Alturki A, Feng F, Nair A, Guntu V, Nair SS (2016) Distinct current modules shape cellular dynamics in model neurons. Neuroscience 334:309-331 [Journal] [PubMed]

   Distinct current modules shape cellular dynamics in model neurons (Alturki et al 2016) [Model]

(96 refs)