Cell-Type Specificity of Callosally Evoked Excitation and Feedforward Inhibition in the Prefrontal Cortex

Paul G. Anastasiades, Joseph J. Marlin, Adam Carter

Research output: Contribution to journalArticle

Abstract

Excitation and inhibition are highly specific in the cortex, with distinct synaptic connections made onto subtypes of projection neurons. The functional consequences of this selective connectivity depend on both synaptic strength and the intrinsic properties of targeted neurons but remain poorly understood. Here, we examine responses to callosal inputs at cortico-cortical (CC) and cortico-thalamic (CT) neurons in layer 5 of mouse prelimbic prefrontal cortex (PFC). We find callosally evoked excitation and feedforward inhibition are much stronger at CT neurons compared to neighboring CC neurons. Elevated inhibition at CT neurons reflects biased synaptic inputs from parvalbumin and somatostatin positive interneurons. The intrinsic properties of postsynaptic targets equalize excitatory and inhibitory response amplitudes but selectively accelerate decays at CT neurons. Feedforward inhibition further reduces response amplitude and balances action potential firing across these projection neurons. Our findings highlight the synaptic and cellular mechanisms regulating callosal recruitment of layer 5 microcircuits in PFC. Anastasiades et al. explore the functional significance of differences in synaptic connectivity and intrinsic physiology at two classes of layer 5 projection neurons in the prefrontal cortex (PFC). They find subthreshold and suprathreshold responses depend on cell-type-specific connectivity and physiology, which combine to influence synaptic responses and evoked firing.

Original languageEnglish (US)
Pages (from-to)679-692
Number of pages14
JournalCell Reports
Volume22
Issue number3
DOIs
StatePublished - Jan 16 2018

Fingerprint

Prefrontal Cortex
Neurons
Corpus Callosum
Physiology
Parvalbumins
Interneurons
Somatostatin
Action Potentials

Keywords

  • circuits
  • excitation
  • feedforward
  • h-current
  • inhibition
  • interneuron
  • optogenetics
  • prefrontal cortex
  • pyramidal neuron
  • synaptic transmission

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Cell-Type Specificity of Callosally Evoked Excitation and Feedforward Inhibition in the Prefrontal Cortex. / Anastasiades, Paul G.; Marlin, Joseph J.; Carter, Adam.

In: Cell Reports, Vol. 22, No. 3, 16.01.2018, p. 679-692.

Research output: Contribution to journalArticle

Anastasiades, Paul G. ; Marlin, Joseph J. ; Carter, Adam. / Cell-Type Specificity of Callosally Evoked Excitation and Feedforward Inhibition in the Prefrontal Cortex. In: Cell Reports. 2018 ; Vol. 22, No. 3. pp. 679-692.
@article{13c07bcfb8df40bfbd8e193df1bbdb5e,
title = "Cell-Type Specificity of Callosally Evoked Excitation and Feedforward Inhibition in the Prefrontal Cortex",
abstract = "Excitation and inhibition are highly specific in the cortex, with distinct synaptic connections made onto subtypes of projection neurons. The functional consequences of this selective connectivity depend on both synaptic strength and the intrinsic properties of targeted neurons but remain poorly understood. Here, we examine responses to callosal inputs at cortico-cortical (CC) and cortico-thalamic (CT) neurons in layer 5 of mouse prelimbic prefrontal cortex (PFC). We find callosally evoked excitation and feedforward inhibition are much stronger at CT neurons compared to neighboring CC neurons. Elevated inhibition at CT neurons reflects biased synaptic inputs from parvalbumin and somatostatin positive interneurons. The intrinsic properties of postsynaptic targets equalize excitatory and inhibitory response amplitudes but selectively accelerate decays at CT neurons. Feedforward inhibition further reduces response amplitude and balances action potential firing across these projection neurons. Our findings highlight the synaptic and cellular mechanisms regulating callosal recruitment of layer 5 microcircuits in PFC. Anastasiades et al. explore the functional significance of differences in synaptic connectivity and intrinsic physiology at two classes of layer 5 projection neurons in the prefrontal cortex (PFC). They find subthreshold and suprathreshold responses depend on cell-type-specific connectivity and physiology, which combine to influence synaptic responses and evoked firing.",
keywords = "circuits, excitation, feedforward, h-current, inhibition, interneuron, optogenetics, prefrontal cortex, pyramidal neuron, synaptic transmission",
author = "Anastasiades, {Paul G.} and Marlin, {Joseph J.} and Adam Carter",
year = "2018",
month = "1",
day = "16",
doi = "10.1016/j.celrep.2017.12.073",
language = "English (US)",
volume = "22",
pages = "679--692",
journal = "Cell Reports",
issn = "2211-1247",
publisher = "Cell Press",
number = "3",

}

TY - JOUR

T1 - Cell-Type Specificity of Callosally Evoked Excitation and Feedforward Inhibition in the Prefrontal Cortex

AU - Anastasiades, Paul G.

AU - Marlin, Joseph J.

AU - Carter, Adam

PY - 2018/1/16

Y1 - 2018/1/16

N2 - Excitation and inhibition are highly specific in the cortex, with distinct synaptic connections made onto subtypes of projection neurons. The functional consequences of this selective connectivity depend on both synaptic strength and the intrinsic properties of targeted neurons but remain poorly understood. Here, we examine responses to callosal inputs at cortico-cortical (CC) and cortico-thalamic (CT) neurons in layer 5 of mouse prelimbic prefrontal cortex (PFC). We find callosally evoked excitation and feedforward inhibition are much stronger at CT neurons compared to neighboring CC neurons. Elevated inhibition at CT neurons reflects biased synaptic inputs from parvalbumin and somatostatin positive interneurons. The intrinsic properties of postsynaptic targets equalize excitatory and inhibitory response amplitudes but selectively accelerate decays at CT neurons. Feedforward inhibition further reduces response amplitude and balances action potential firing across these projection neurons. Our findings highlight the synaptic and cellular mechanisms regulating callosal recruitment of layer 5 microcircuits in PFC. Anastasiades et al. explore the functional significance of differences in synaptic connectivity and intrinsic physiology at two classes of layer 5 projection neurons in the prefrontal cortex (PFC). They find subthreshold and suprathreshold responses depend on cell-type-specific connectivity and physiology, which combine to influence synaptic responses and evoked firing.

AB - Excitation and inhibition are highly specific in the cortex, with distinct synaptic connections made onto subtypes of projection neurons. The functional consequences of this selective connectivity depend on both synaptic strength and the intrinsic properties of targeted neurons but remain poorly understood. Here, we examine responses to callosal inputs at cortico-cortical (CC) and cortico-thalamic (CT) neurons in layer 5 of mouse prelimbic prefrontal cortex (PFC). We find callosally evoked excitation and feedforward inhibition are much stronger at CT neurons compared to neighboring CC neurons. Elevated inhibition at CT neurons reflects biased synaptic inputs from parvalbumin and somatostatin positive interneurons. The intrinsic properties of postsynaptic targets equalize excitatory and inhibitory response amplitudes but selectively accelerate decays at CT neurons. Feedforward inhibition further reduces response amplitude and balances action potential firing across these projection neurons. Our findings highlight the synaptic and cellular mechanisms regulating callosal recruitment of layer 5 microcircuits in PFC. Anastasiades et al. explore the functional significance of differences in synaptic connectivity and intrinsic physiology at two classes of layer 5 projection neurons in the prefrontal cortex (PFC). They find subthreshold and suprathreshold responses depend on cell-type-specific connectivity and physiology, which combine to influence synaptic responses and evoked firing.

KW - circuits

KW - excitation

KW - feedforward

KW - h-current

KW - inhibition

KW - interneuron

KW - optogenetics

KW - prefrontal cortex

KW - pyramidal neuron

KW - synaptic transmission

UR - http://www.scopus.com/inward/record.url?scp=85041694518&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85041694518&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2017.12.073

DO - 10.1016/j.celrep.2017.12.073

M3 - Article

C2 - 29346766

AN - SCOPUS:85041694518

VL - 22

SP - 679

EP - 692

JO - Cell Reports

JF - Cell Reports

SN - 2211-1247

IS - 3

ER -