Induction of theta-frequency oscillations in the rat medial septal diagonal band slice by metabotropic glutamate receptor agonists

Lu, Chengbiao; Ouyang, Gaoxiang; Henderson, Z.; Li, X.

doi:10.1016/j.neuroscience.2011.01.004

Cited by 12 publications

(7 citation statements)

References 48 publications

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“…We found a substantial increase in the firing rates in MS pacemaker neurons upon theta onset. This finding is in line with previous studies suggesting that an increased tonic excitatory drive can switch the MS network into theta state (Korvasova ´et al, 2021;Lu et al, 2011;M€ uller and Remy, 2018;Oddie et al, 1996;Ujfalussy and Kiss, 2006). Multiple cell types and pathways were proposed to contribute to this excitatory drive, including MS cholinergic, glutamatergic, and ascending brainstem inputs (Hajszan et al, 2004;Leranth and Frotscher, 1989; M€ uller and Remy, 2018; Oddie and Bland, 1998;Zaborszky et al, 2012).…”

Section: Discussionsupporting

confidence: 91%

Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

et al. 2022

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Section: Discussionsupporting

confidence: 91%

Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

et al. 2022

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“…We found a substantial elevation of firing rates in MS pacemaker neurons upon theta onset. This finding is in line with previous suggestions that an increased tonic excitatory drive can switch the MS network into theta state (Lu et al, 2011;Müller and Remy, 2018;Oddie et al, 1996;Ujfalussy and Kiss, 2006).…”

Section: Discussionsupporting

confidence: 93%

Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

Kocsis

Martínez-Bellver

Fiáth

et al. 2021

Preprint

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Episodic learning and memory retrieval are critically dependent on a hippocampal 4-12 Hz oscillatory ‘clock’ signal, the theta oscillation. This clock is largely externally paced, by a network of GABAergic neurons in the medial septum (MS). Theoretical studies suggested a range of hypotheses how this network may achieve theta synchrony; however, experimental evidence is still lacking. By recording multiple single MS neurons and hippocampal local field potential oscillations simultaneously, with both acute and chronically implanted silicon probes, we show that MS pacemaker units oscillate at individual frequencies within the theta range in rodents. Synchronization of MS neuron frequencies, accompanied by an elevation of firing rates, was found to parallel hippocampal theta formation in multiple rodent model systems. This suggests a general mechanism for theta synchronization, akin to the synchronization of weakly coupled pendulum clocks observed by Huygens in the 17th century. We optogenetically identified the MS pacemaker units as parvalbumin-expressing GABAergic neurons, while the previously enigmatic MS glutamatergic neurons were mostly theta-activated non-rhythmic cells. Our data were consistent with a network model of partially connected single-compartment inhibitory pacemaker neurons, in which synchronization and de-synchronization in the frequency domain upon waxing and waning tonic excitatory drive was sufficient to toggle MS network output between theta and non-theta states. These results provide experimental and theoretical support to a frequency-synchronization mechanism for pacing hippocampal theta, which may serve as an inspirational prototype for the countless examples of synchronization processes in the central nervous system from Nematoda to Anthropoda to Chordate and Vertebrate phyla.

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“…Activation of either mGluR1 or kainite receptor induced γ oscillations in hippocampal slices [10,11] , but it only induced θ oscillations in MSDB slices [12,13] , suggesting that the local circuit of the neuronal network for the generation of rhythmic activity between the hippocampus and the MSDB are different.…”

Section: Introductionmentioning

confidence: 97%

Co-activation of nAChR and mGluR induces γ oscillation in rat medial septum diagonal band of Broca slices

Wang

Ouyang

et al. 2014

Acta Pharmacol Sin

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Aim: To examine whether co-activation of nAChR and mGluR1 induced γ oscillation (20-60 Hz) in rat medial septum diagonal band of Broca (MSDB) slices. Methods: Rat brain sagittal slices containing the MSDB were prepared. Extracellular field potentials were recorded with glass microelectrodes. The nAChR and mGluR1 agonists were applied to the slices to induce network activity. Data analysis was performed off-line using software Spike 2. Results: Co-application of the nAChR agonist nicotine (1 µmol/L) and the mGluR1 agonist dihydroxyphenylglycine (DHPG, 25 µmol/L) was able to induce γ oscillation in MSDB slices. The intensity of nAChR and mGluR1 activation was critical for induction of network oscillation at a low (θ oscillation) or high frequency (γ oscillation): co-application of low concentrations of the two agonists only increased the power and frequency of oscillation within the range of θ, whereas γ oscillation mostly appeared when high concentrations of the two agonists were applied. Conclusion: Activation of mGluR1 and nAChR is able to program slow or fast network oscillation by altering the intensity of receptor activation, which may provide a mechanism for modulation of learning and memory.

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Induction of theta-frequency oscillations in the rat medial septal diagonal band slice by metabotropic glutamate receptor agonists

Cited by 12 publications

References 48 publications

Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

Co-activation of nAChR and mGluR induces γ oscillation in rat medial septum diagonal band of Broca slices

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