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.

Original languageEnglish (US)
Pages (from-to)369-389
Number of pages21
JournalJournal of Computational Neuroscience
Volume34
Issue number3
DOIs
StatePublished - Jun 1 2013

Fingerprint

Interneurons
Hippocampal CA1 Region
Pyramidal Cells
Cognition
Neurons
Gamma Rhythm
Inhibition (Psychology)

All Science Journal Classification (ASJC) codes

  • Sensory Systems
  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

Cite this

@article{18b23efc03714eaabc221b818529b322,
title = "Modulation of hippocampal rhythms by subthreshold electric fields and network topology",
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.",
author = "Julia Berzhanskaya and Nick Chernyy and Bruce Gluckman and Steven Schiff and Ascoli, {Giorgio A.}",
year = "2013",
month = "6",
day = "1",
doi = "10.1007/s10827-012-0426-4",
language = "English (US)",
volume = "34",
pages = "369--389",
journal = "Journal of Computational Neuroscience",
issn = "0929-5313",
publisher = "Springer Netherlands",
number = "3",

}

Modulation of hippocampal rhythms by subthreshold electric fields and network topology. / Berzhanskaya, Julia; Chernyy, Nick; Gluckman, Bruce; Schiff, Steven; Ascoli, Giorgio A.

In: Journal of Computational Neuroscience, Vol. 34, No. 3, 01.06.2013, p. 369-389.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Modulation of hippocampal rhythms by subthreshold electric fields and network topology

AU - Berzhanskaya, Julia

AU - Chernyy, Nick

AU - Gluckman, Bruce

AU - Schiff, Steven

AU - Ascoli, Giorgio A.

PY - 2013/6/1

Y1 - 2013/6/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84877771040&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84877771040&partnerID=8YFLogxK

U2 - 10.1007/s10827-012-0426-4

DO - 10.1007/s10827-012-0426-4

M3 - Article

C2 - 23053863

AN - SCOPUS:84877771040

VL - 34

SP - 369

EP - 389

JO - Journal of Computational Neuroscience

JF - Journal of Computational Neuroscience

SN - 0929-5313

IS - 3

ER -