Journal of Computational Neuroscience

, Volume 34, Issue 3, pp 369–389 | Cite as

Modulation of hippocampal rhythms by subthreshold electric fields and network topology

  • Julia Berzhanskaya
  • Nick Chernyy
  • Bruce J. Gluckman
  • Steven J. Schiff
  • Giorgio A. Ascoli
Article

Abstract

Theta (4–12 Hz) and gamma (30–80 Hz) rhythms are considered important for cortical and hippocampal function. Although several neuron types are implicated in rhythmogenesis, the exact cellular mechanisms remain unknown. Subthreshold electric fields provide a flexible, area-specific tool to modulate neural activity and directly test functional hypotheses. Here we present experimental and computational evidence of the interplay among hippocampal synaptic circuitry, neuronal morphology, external electric fields, and network activity. Electrophysiological data are used to constrain and validate an anatomically and biophysically realistic model of area CA1 containing pyramidal cells and two interneuron types: dendritic- and perisomatic-targeting. We report two lines of results: addressing the network structure capable of generating theta-modulated gamma rhythms, and demonstrating electric field effects on those rhythms. First, theta-modulated gamma rhythms require specific inhibitory connectivity. In one configuration, GABAergic axo-dendritic feedback on pyramidal cells is only effective in proximal but not distal layers. An alternative configuration requires two distinct perisomatic interneuron classes, one exclusively receiving excitatory contacts, the other additionally targeted by inhibition. These observations suggest novel roles for particular classes of oriens and basket cells. The second major finding is that subthreshold electric fields robustly alter the balance between different rhythms. Independent of network configuration, positive electric fields decrease, while negative fields increase the theta/gamma ratio. Moreover, electric fields differentially affect average theta frequency depending on specific synaptic connectivity. These results support the testable prediction that subthreshold electric fields can alter hippocampal rhythms, suggesting new approaches to explore their cognitive functions and underlying circuitry.

Keywords

Pyramidal Interneuron Theta-rhythm Gamma-rhythm 

Abbreviations:

Notation

CA1

cornus ammonis area 1

CA3

cornus ammonis area 3

SC

Schaffer Collateral

alv.

alveus

s.o.

stratum oriens

s.p.

stratum pyramidale

s.r.

stratum radiatum

s.l.m.

stratum lacunosum moleculare

O-bi

Oriens-bistratified

OLM

Oriens-lacunosum moleculare

ISI

interspike interval

IBI

interburst interval

CCK

Cholecystokinin

IPSC/IPSP

Inhibitory postsynaptic currents/potentials

EPSC/EPSP

Excitatory postsynaptic currents/potentials

GABA

4-aminobutanoic acid

AMPA

alpha- Amino −3 hydroxyl −5 Methyl- 4- isoxazole-Propanoic acid

NMDA

N-Methyl-D-aspartic acid

Network model

P

pyramidal cell (excitatory)

O

oriens cell (inhibitory, dendritic targeting, O-Bi/OLM)

B

basket cell (inhibitory, perisomatic targeting, B1/B2)

OBp

Network configuration with strong O-B connections and weak O-P connections

OPb

Network configuration with weak O-B connections and strong O-P connections

B-vert

basket cell with vertically oriented dendrites

O-vert

oriens cell with vertically oriented dendrites

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Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Julia Berzhanskaya
    • 1
  • Nick Chernyy
    • 2
  • Bruce J. Gluckman
    • 3
  • Steven J. Schiff
    • 4
  • Giorgio A. Ascoli
    • 1
  1. 1.Center for Neural Informatics, Structures, & Plasticity, and Molecular Neuroscience Department; Krasnow Institute for Advanced StudyGeorge Mason UniversityFairfaxUSA
  2. 2.Center for Neural Engineering, Departments of Engineering Science and MechanicsPenn State UniversityUniversity ParkUSA
  3. 3.Center for Neural Engineering, Departments of Engineering Science and Mechanics, Neurosurgery and BioengineeringPenn State UniversityUniversity ParkUSA
  4. 4.Center for Neural Engineering, Departments of Engineering Science and Mechanics, Neurosurgery and PhysicsPenn State UniversityUniversity ParkUSA

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