scholarly journals Huygens synchronization of medial septal pacemaker neurons generates hippocampal theta oscillation

2021 ◽  
Author(s):  
Barnabás Kocsis ◽  
Sergio Martínez-Bellver ◽  
Richárd Fiáth ◽  
Andor Domonkos ◽  
Katalin Sviatkó ◽  
...  
Keyword(s):  
Field Potential ◽  
Medial Septum ◽  
Gabaergic Neurons ◽  
Model Systems ◽  
General Mechanism ◽  
Clock Signal ◽  
Pacemaker Neurons ◽  
Potential Oscillations ◽  
Theta Oscillation ◽  
Hippocampal Theta

AbstractEpisodic 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.

scholarly journals Interconnection and synchronization of neuronal populations in the mouse medial septum/diagonal band of Broca

2015 ◽  
Vol 113 (3) ◽  
pp. 971-980 ◽  
Author(s):  
Richardson N. Leão ◽  
Zé H. Targino ◽  
Luis V. Colom ◽  
André Fisahn
Keyword(s):  
Action Potentials ◽  
Theta Rhythm ◽  
Medial Septum ◽  
Gabaergic Neurons ◽  
Action Potential Firing ◽  
Neuronal Populations ◽  
Diagonal Band ◽  
Potential Firing ◽  
Diagonal Band Of Broca ◽  
Hippocampal Theta

The medial septum/diagonal band of Broca (MS/DBB) is crucial for hippocampal theta rhythm generation (4–12 Hz). However, the mechanisms behind theta rhythmogenesis are still under debate. The MS/DBB consists, in its majority, of three neuronal populations that use acetylcholine, GABA, or glutamate as neurotransmitter. While the firing patterns of septal neurons enable the MS/DBB to generate rhythmic output critical for the generation of the hippocampal theta rhythm, the ability to synchronize these action potentials is dependent on the interconnectivity between the three major MS/DBB neuronal populations, yet little is known about intraseptal connections. Here we assessed the connectivity between pairs of MS/DBB neurons with paired patch-clamp recordings. We found that glutamatergic and GABAergic neurons provide intraseptal connections and produce sizable currents in MS/DBB postsynaptic cells. We also analyzed linear and nonlinear relationships between the action potentials fired by pairs of neurons belonging to various MS/DBB neuronal populations. Our results show that while the synchrony index for action potential firing was significantly higher in pairs of GABAergic neurons, coherence of action potential firing in the theta range was similarly low in all pairs analyzed. Recurrence analysis demonstrated that individual action potentials were more recurrent in cholinergic neurons than in other cell types. Implementing sparse connectivity in a computer model of the MS/DBB network reproduced our experimental data. We conclude that the interplay between the intrinsic membrane properties of different MS/DBB neuronal populations and the connectivity among these populations underlie the ability of the MS/DBB network to critically contribute to hippocampal theta rhythmogenesis.

scholarly journals Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

2019 ◽  
Author(s):  
Justin Losacco ◽  
Daniel Ramirez-Gordillo ◽  
Jesse Gilmer ◽  
Diego Restrepo
Keyword(s):  
Olfactory Bulb ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Brain Regions ◽  
Spike Timing ◽  
Potential Oscillations ◽  
Theta Oscillation ◽  
Beta Power ◽  
Early Processing ◽  
Theta Phase

AbstractLocal field potential oscillations reflect temporally coordinated neuronal ensembles— coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.SignificanceEarly processing of olfactory information takes place in circuits undergoing slow frequency theta oscillations generated by the interplay of olfactory input modulated by sniffing and centrifugal feedback from downstream brain areas. Studies in the hippocampus and cortex suggest that different information “chunks” are conveyed at different phases of the theta oscillation. Here we show that in the olfactory bulb, the first processing station in the olfactory system, the amplitude of high frequency gamma oscillations encodes for information on whether an odorant is rewarded when it is observed at the peak phase of the theta oscillation. Furthermore, encoding of information by the theta phase-referenced gamma oscillations becomes more accurate as the animal learns to differentiate two odorants.

Loss of Rhythmically Bursting Neurons in Rat Medial Septum Following Selective Lesion of Septohippocampal Cholinergic System

1998 ◽  
Vol 79 (4) ◽  
pp. 1633-1642 ◽  
Author(s):  
Emmanuelle Apartis ◽  
Frederique R. Poindessous-Jazat ◽  
Yvon A. Lamour ◽  
Marie H. Bassant
Keyword(s):  
Cholinergic System ◽  
Hippocampal Formation ◽  
Paradoxical Sleep ◽  
Significant Proportion ◽  
Medial Septum ◽  
Gabaergic Neurons ◽  
Bursting Neurons ◽  
Selective Lesion ◽  
Hippocampal Theta ◽  
Septal Neurons

Apartis, Emmanuelle, Frederique R. Poindessous-Jazat, Yvon A. Lamour, and Marie H. Bassant. Loss of rhythmically bursting neurons in rat medial septum following selective lesion of septohippocampal cholinergic system. J. Neurophysiol. 79: 1633–1642, 1998. The medial septum contains cholinergic and GABAergic neurons that project to the hippocampal formation. A significant proportion of the septohippocampal neurons (SHN) exhibit a rhythmically bursting (RB) activity that is involved in the generation of the hippocampal theta rhythm. The neurochemical nature of septal RB neurons is not firmly established. To address this question, the septal unit activity has been recorded in rats after selective destruction of the cholinergic septal neurons by the immunotoxin 192 IgG-saporin. Experiments have been performed in urethan-anesthetized and unanesthetized rats, 14–21 days after lesion. Acetylcholinesterase (AChE) histochemistry revealed a near-complete loss of cholinergic septal neurons and of cholinergic fibers in the hippocampus. The recorded neurons were located in the medial septum-diagonal band of Broca area. A number of these neurons were identified as projecting to the hippocampus (SHN) by their antidromic response to the electrical stimulation of the fimbria-fornix. In urethan-anesthetized lesioned rats, the percentage of RB neurons decreased significantly as compared with controls (17 vs. 41% for SHNs and 5 vs. 19% for unidentified septal neurons). The axonal conduction velocity and the burst frequency of the SHNs that retained a RB activity were higher in lesioned as compared with control rats. The number of spikes per burst was lower and the burst duration was shorter in lesioned rats as compared with controls. The urethan-resistant hippocampal theta was altered both in terms of frequency and amplitude. In unanesthetized lesioned rats, no RB septal neurons were found during arousal, as compared with 25% in controls. Their number was also markedly reduced during paradoxical sleep (9.7 vs. 38.5%). Histochemistry in 192 IgG-saporin–treated rats showed that RB neurons were found in areas devoid of AChE-positive neurons but containing parvalbumine-positive (presumably GABAergic) neurons. These data show that RB activity is considerably reduced after selective lesion of the cholinergic medial septal neurons. They suggested that the large majority of the RB septal neurons are cholinergic and that the few neurons that display RB activity in lesioned rats are GABAergic.

scholarly journals Huygens Synchronization of Medial Septal Pacemaker Neurons Generates Hippocampal Theta Oscillation

2021 ◽  
Author(s):  
Barnabás Kocsis ◽  
Sergio Martínez-Bellver ◽  
Richárd Fiáth ◽  
Andor Domonkos ◽  
Katalin Sviatkó ◽  
...  
Keyword(s):  
Pacemaker Neurons ◽  
Theta Oscillation ◽  
Hippocampal Theta

scholarly journals Crucial Role of FABP3 in αSyn-Induced Reduction of Septal GABAergic Neurons and Cognitive Decline in Mice

2021 ◽  
Vol 22 (1) ◽  
pp. 400
Author(s):  
Kazuya Matsuo ◽  
Yasushi Yabuki ◽  
Ronald Melki ◽  
Luc Bousset ◽  
Yuji Owada ◽  
...  
Keyword(s):  
Cognitive Impairment ◽  
Cognitive Decline ◽  
Cognitive Processing ◽  
Dopaminergic Neurons ◽  
Dorsal Striatum ◽  
Cholinergic Neurons ◽  
Medial Septum ◽  
Gabaergic Neurons ◽  
Gamma Aminobutyric Acid ◽  
Fatty Acid Binding

In synucleinopathies, while motor symptoms are thought to be attributed to the accumulation of misfolded α-synuclein (αSyn) in nigral dopaminergic neurons, it remains to be elucidated how cognitive decline arises. Here, we investigated the effects of distinct αSyn strains on cognition and the related neuropathology in the medial septum/diagonal band (MS/DB), a key region for cognitive processing. Bilateral injection of αSyn fibrils into the dorsal striatum potently impaired cognition in mice. The cognitive decline was accompanied by accumulation of phosphorylated αSyn at Ser129 and reduction of gamma-aminobutyric acid (GABA)-ergic but not cholinergic neurons in the MS/DB. Since we have demonstrated that fatty acid-binding protein 3 (FABP3) is critical for αSyn neurotoxicity in nigral dopaminergic neurons, we investigated whether FABP3 also participates in αSyn pathology in the MS/DB and cognitive decline. FABP3 was highly expressed in GABAergic but rarely in cholinergic neurons in the MS/DB. Notably, Fabp3 deletion antagonized the accumulation of phosphorylated αSyn, decrease in GABAergic neurons, and cognitive impairment caused by αSyn fibrils. Overall, the present study indicates that FABP3 mediates αSyn neurotoxicity in septal GABAergic neurons and the resultant cognitive impairment, and that FABP3 in this subpopulation could be a therapeutic target for dementia in synucleinopathies.

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