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Modulation of hippocampal rhythms by subthreshold electric fields and network topology

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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.

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Abbreviations

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

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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Acknowledgments

The authors are thankful to Drs. C. McIntyre and M. Robertson for sharing initial code of extracellular electric field implementation in NEURON, Dr. John L. Baker and Mr. Kerry Brown for feedback on a previous version of the manuscript, and financial support from NIH grants R01 MH50006, K02 MH01493, R01 NS39600, R01 AG25633, R21 NS58816, and ONR grant MURI N00014-10-1-0198.

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Authors and Affiliations

  1. Center for Neural Informatics, Structures, & Plasticity, and Molecular Neuroscience Department; Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA, USA

    Julia Berzhanskaya & Giorgio A. Ascoli

  2. Center for Neural Engineering, Departments of Engineering Science and Mechanics, Penn State University, University Park, PA, USA

    Nick Chernyy

  3. Center for Neural Engineering, Departments of Engineering Science and Mechanics, Neurosurgery and Bioengineering, Penn State University, University Park, PA, USA

    Bruce J. Gluckman

  4. Center for Neural Engineering, Departments of Engineering Science and Mechanics, Neurosurgery and Physics, Penn State University, University Park, PA, USA

    Steven J. Schiff

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  5. Giorgio A. Ascoli
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Correspondence to Giorgio A. Ascoli.

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Berzhanskaya, J., Chernyy, N., Gluckman, B.J. et al. Modulation of hippocampal rhythms by subthreshold electric fields and network topology. J Comput Neurosci 34, 369–389 (2013). https://doi.org/10.1007/s10827-012-0426-4

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  • DOI: https://doi.org/10.1007/s10827-012-0426-4

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