Cholinergic control in developing prefrontal-hippocampal networks.
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Cholinergic control in developing prefrontal-hippocampal networks. / Janiesch, Phillipp Christoph; Krüger, Hanna-Sophie; Pöschel, Beatrice; Hanganu-Opatz, Ileana.
in: J NEUROSCI, Jahrgang 31, Nr. 49, 49, 2012, S. 17955-17970.Publikationen: SCORING: Beitrag in Fachzeitschrift/Zeitung › SCORING: Zeitschriftenaufsatz › Forschung › Begutachtung
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TY - JOUR
T1 - Cholinergic control in developing prefrontal-hippocampal networks.
AU - Janiesch, Phillipp Christoph
AU - Krüger, Hanna-Sophie
AU - Pöschel, Beatrice
AU - Hanganu-Opatz, Ileana
PY - 2012
Y1 - 2012
N2 - The cholinergic drive enhances input processing in attentional and mnemonic context by interacting with the activity of prefrontal-hippocampal networks. During development, acetylcholine modulates neuronal proliferation, differentiation, and synaptic plasticity, yet its contribution to the maturation of cognitive processing resulting from early entrainment of neuronal networks in oscillatory rhythms remains widely unknown. Here we show that cholinergic projections growing into the rat prefrontal cortex (PFC) toward the end of the first postnatal week boost the generation of nested gamma oscillations superimposed on discontinuous spindle bursts by acting on functional muscarinic but not nicotinic receptors. Although electrical stimulation of cholinergic nuclei increased the occurrence of nested gamma spindle bursts by 41%, diminishment of the cholinergic input by either blockade of the receptors or chronic immunotoxic lesion had the opposite effect. This activation of locally generated gamma episodes by direct cholinergic projections to the PFC was accompanied by indirect modulation of underlying spindle bursts via cholinergic control of hippocampal theta activity. With ongoing maturation and switch of network activity from discontinuous bursts to continuous theta-gamma rhythms, accumulating cholinergic projections acting on both muscarinic and nicotinic receptors mediated the transition from high-amplitude slow to low-amplitude fast rhythms in the PFC. By exerting multiple actions on the oscillatory entrainment of developing prefrontal-hippocampal networks, the cholinergic input may refine them for later gating processing in executive and mnemonic tasks.
AB - The cholinergic drive enhances input processing in attentional and mnemonic context by interacting with the activity of prefrontal-hippocampal networks. During development, acetylcholine modulates neuronal proliferation, differentiation, and synaptic plasticity, yet its contribution to the maturation of cognitive processing resulting from early entrainment of neuronal networks in oscillatory rhythms remains widely unknown. Here we show that cholinergic projections growing into the rat prefrontal cortex (PFC) toward the end of the first postnatal week boost the generation of nested gamma oscillations superimposed on discontinuous spindle bursts by acting on functional muscarinic but not nicotinic receptors. Although electrical stimulation of cholinergic nuclei increased the occurrence of nested gamma spindle bursts by 41%, diminishment of the cholinergic input by either blockade of the receptors or chronic immunotoxic lesion had the opposite effect. This activation of locally generated gamma episodes by direct cholinergic projections to the PFC was accompanied by indirect modulation of underlying spindle bursts via cholinergic control of hippocampal theta activity. With ongoing maturation and switch of network activity from discontinuous bursts to continuous theta-gamma rhythms, accumulating cholinergic projections acting on both muscarinic and nicotinic receptors mediated the transition from high-amplitude slow to low-amplitude fast rhythms in the PFC. By exerting multiple actions on the oscillatory entrainment of developing prefrontal-hippocampal networks, the cholinergic input may refine them for later gating processing in executive and mnemonic tasks.
KW - Animals
KW - Male
KW - Female
KW - Age Factors
KW - Rats
KW - Electric Stimulation
KW - Rats, Wistar
KW - Animals, Newborn
KW - Pregnancy
KW - Nerve Tissue Proteins/metabolism
KW - Choline O-Acetyltransferase/metabolism
KW - Antibodies, Monoclonal/pharmacology
KW - Neurons/physiology
KW - Action Potentials/drug effects/physiology
KW - Cholinergic Agents/metabolism
KW - Gene Expression Regulation, Developmental/drug effects/physiology
KW - Hippocampus/cytology/drug effects/growth & development
KW - Neural Pathways/drug effects/physiology
KW - Prefrontal Cortex/cytology/drug effects/growth & development
KW - Protein Binding/drug effects
KW - Ribosome Inactivating Proteins, Type 1/pharmacology
KW - gamma-Aminobutyric Acid/metabolism
KW - Animals
KW - Male
KW - Female
KW - Age Factors
KW - Rats
KW - Electric Stimulation
KW - Rats, Wistar
KW - Animals, Newborn
KW - Pregnancy
KW - Nerve Tissue Proteins/metabolism
KW - Choline O-Acetyltransferase/metabolism
KW - Antibodies, Monoclonal/pharmacology
KW - Neurons/physiology
KW - Action Potentials/drug effects/physiology
KW - Cholinergic Agents/metabolism
KW - Gene Expression Regulation, Developmental/drug effects/physiology
KW - Hippocampus/cytology/drug effects/growth & development
KW - Neural Pathways/drug effects/physiology
KW - Prefrontal Cortex/cytology/drug effects/growth & development
KW - Protein Binding/drug effects
KW - Ribosome Inactivating Proteins, Type 1/pharmacology
KW - gamma-Aminobutyric Acid/metabolism
M3 - SCORING: Journal article
VL - 31
SP - 17955
EP - 17970
JO - J NEUROSCI
JF - J NEUROSCI
SN - 0270-6474
IS - 49
M1 - 49
ER -
