Alina Vazetdinova

Kazan Federal University

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Andrei Rozov

N. I. Lobachevsky State University of Nizhny Novgorod

Azat Nasretdinov

Kazan Federal University

Fliza Valiullina-Rakhmatullina

Kazan Federal University

David Jappy

Research Center of Neurology

Viktoria Krut

Federal Center of Brain Research and Neurotechnologies

Yulia Dobryakova

Institute of Higher Nervous Activity and Neurophysiology

Julia Lebedeva

Kazan Federal University

Marina Eliava

Heidelberg University

Rostislav I. Sokolov

Pirogov Russian National Research Medical University

Valery Grinevich

Central Institute of Mental Health

Cooperative Institutions

Heidelberg University

Kazan Federal University

Research Center of Neurology

N. I. Lobachevsky State University of Nizhny Novgorod

Federal Center of Brain Research and Neurotechnologies

Central Institute of Mental Health

University Hospital Heidelberg

Max Planck Institute for Medical Research

Heidelberg University

Federal Medical-Biological Agency

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Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Julia Lebedeva David Jappy Azat Nasretdinov Alina Vazetdinova Viktoria Krut

For over half a century, it has been postulated that the internal excitatory circuit in the hippocampus consists of three relay stations. Excitation arrives from the entorhinal cortex to the DG granule cells, is transmitted through the mossy fibers to CA3 pyramidal cells, and is then transmitted through Schaffer collaterals to CA1 pyramidal neurons. In all three structures (DG, CA3 and CA1), the activity of the excitatory neurons involved in the synaptic transmission of excitation are under the control of inhibitory basket neurons that are recruited into network activity via feed-forward and feed-back excitation. However, in the late 90s “stratum radiatum giant cells” were described as a novel type of neuron with the anatomical features of excitatory cells. Since then, the role of these cells in the hippocampal circuitry has not been well understood. Here, using optogenetic and electrophysiological techniques we characterized the functional location of these neurons within the hippocampal network. We show that: (i) the main excitatory drive to giant excitatory neurons in stratum radiatum (ExN R ) comes via Schaffer collaterals; (ii) within the CA1 field, ExN R are not directly connected with local pyramidal cells, but provide massive and efficient excitatory input to parvalbumin positive (PV+) interneurons; (iii) ExN R are reciprocally innervated by bistratified cells, but not inhibited by backet interneurons; (iv) the efficiency of ExN R excitation to PV+ interneurons is sufficient for a single ExN R action potential to trigger massive inhibition of downstream CA1 pyramidal cells. Taken together, our data shows that ExN R constitute an alternative pathway of excitation for CA1 interneurons that avoids the burden of perisomatic inhibition.

Stratum

10.7554/elife.94385

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The Role of Polyamine-Dependent Facilitation of Calcium Permeable AMPARs in Short-Term Synaptic Enhancement

Frontiers in Cellular Neuroscience (2018)

Andrei Rozov Yulia Zakharova Alina Vazetdinova Fliza Valiullina-Rakhmatullina

Depending on subunit composition AMPA receptor channels can be subdivided into two groups: GluA2-containing calcium impermeable AMPARs, and GluA2-lacking calcium permeable, AMPARs. These two groups differ in a number of biophysical properties and, most likely, in their functional role at glutamatergic synapses. GluA2-lacking channels have received a lot of attention over the last two decades mainly due to high calcium permeability, which was suggested to play a significant role in the induction of long-term synaptic plasticity in healthy tissue and neuronal death under neuropathological conditions. However, calcium permeable AMPARs possess another property that can contribute substantially to frequency dependent dynamics of synaptic efficacy. In the closed state calcium permeable AMPARs are blocked by endogenous polyamines, however, repetitive activation leads to progressive relief from the block and to the facilitation of ion flux through these channels. Polyamine-dependent facilitation of AMPARs can contribute to short-term plasticity at synapses that have high initial release probability and express calcium permeable AMPARs. During synaptic transmission activity-dependent relief from polyamine block of postsynaptic calcium-permeable AMPARs either counteracts presynaptic short-term depression in a frequency-dependent manner or, under specific stimulation conditions, induces facilitation of a synaptic response. Taking into account the fact that expression of calcium permeable AMPARs is developmentally regulated, depends on network activity and increases in diseased brain states, polyamine-dependent facilitation of calcium permeable AMPARs is an important, entirely postsynaptic mechanism of synaptic gain regulation.

Neural facilitation

Nonsynaptic plasticity

Facilitation

Synaptic scaling

Polyamine

10.3389/fncel.2018.00345

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Citations (14)

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Julia Lebedeva David Jappy Azat Nasretdinov Alina Vazetdinova Viktoria Krut

Stratum

10.7554/elife.94385.1

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Citations (1)

On the accuracy of cell-attached current-clamp recordings from cortical neurons

Frontiers in Molecular Neuroscience (2022)

Alina Vazetdinova Fliza Valiullina-Rakhmatullina Andrei Rozov Alexander Evstifeev Roustem Khazipov

Cell-attached current-clamp (CA/CC) recordings have been proposed to measure resting membrane potential and synaptic/agonist responses in neurons without disrupting the cell membrane, thus avoiding the intracellular dialysis that occurs in conventional whole-cell recordings (WC). However, the accuracy of CA/CC recordings in neurons has not been directly assessed. Here, we used concomitant CA and WC current clamp recordings from cortical neurons in brain slices. Resting membrane potential values and slow voltage shifts showed variability and were typically attenuated during CA/CC recordings by ~10-20% relative to WC values. Fast signals were slowed down and their amplitude was greatly reduced: synaptic potentials by nearly 2-fold, and action potentials by nearly 10-fold in CA/CC mode compared to WC. The polarity of GABAergic postsynaptic responses in CA/CC mode matched the responses in WC, and depolarising GABAergic potentials were predominantly observed during CA/CC recordings of intact neonatal CA3 hippocampal pyramidal neurons. Similarly, CA/CC recordings reliably detected neuronal depolarization and excitation during network-induced giant depolarizing potentials in the neonatal CA3 hippocampus, and revealed variable changes, from depolarization to hyperpolarization, in CA1 pyramidal cells during sharp wave ripples in the adult hippocampus. Thus, CA/CC recordings are suitable for assessing membrane potential but signal distortion, probably caused by leakage via the seal contact and RC filtering should be considered.

Current clamp

Reversal potential

Hyperpolarization

Afterhyperpolarization

10.3389/fnmol.2022.979479

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Dialectics of perisomatic inhibition—The unity and conflict of opposites

Frontiers in Neural Circuits (2024)

Andrei Rozov David Jappy Ksenia Maltseva Alina Vazetdinova Fliza Valiullina-Rakhmatullina

Over the past three decades, a great deal of attention has been paid to the study of perisomatic inhibition and perisomatic inhibitory basket cells. A growing body of experimental evidence points to the leading role of perisomatic inhibitory cells in the generation of oscillatory activity in various frequency ranges. Recently the link between the activity of basket cells and complex behavior has been demonstrated in several laboratories. However, all this is true only for one type of perisomatic inhibitory interneuron-parvalbumin-positive basket cells. Nevertheless, where parvalbumin-positive basket cells are found, there is another type of basket cell, cholecystokinin-positive interneurons. These two types of interneurons share a number of common features: they innervate the same compartments of target neurons and they often receive excitation from the same sources, but they also differ from each other in the synchrony of their GABA release and expression of receptors. The functional role of cholecystokinin-positive basket cells in oscillatory activity is not so obvious. They were thought to be involved in theta oscillations, however recent measurements in free moving animals have put some doubts on this hypothesis. Therefore, an important question is, whether these two types of basket cells work synergistically or perform opposing actions in functional networks? In this mini-review, we attempt to answer this question by putting forward the idea that these two types of basket cells are functionally united as two entities of the same network, and their opposing actions are necessary to maintain rhythmogenesis in a "healthy", physiological range.

Dialectic

10.3389/fncir.2024.1494300

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Acute stress modulates hippocampal to entorhinal cortex communication

Frontiers in Cellular Neuroscience (2023)

Azat Nasretdinov David Jappy Alina Vazetdinova Fliza Valiullina-Rakhmatullina Andrei Rozov

Feed-forward inhibition is vital in the transfer and processing of synaptic information within the hippocampal-entorhinal loop by controlling the strength and direction of excitation flow between different neuronal populations and individual neurons. While the cellular targets in the hippocampus that receive excitatory inputs from the entorhinal cortex have been well studied, and the role of feedforward inhibitory neurons has been attributed to neurogliafom cells, the cortical interneurons providing feed-forward control over receiving layer V in the entorhinal cortex remain unknown. We used sharp-wave ripple oscillations as a natural excitatory stimulus of the entorhinal cortex, driven by the hippocampus, to study the function of synaptic interactions between neurons in the deep layers of the entorhinal cortex. We discovered that CB1R-expressing interneurons in the deep layers of the entorhinal cortex constitute the major relay station that translates hippocampal excitation into efficient inhibition of cortical pyramidal cells. The impact of inhibition provided by these interneurons is under strong endocannabinoid control and can be drastically reduced either by enhanced activity of postsynaptic targets or by stress-induced elevation of cannabinoids.

Entorhinal cortex

10.3389/fncel.2023.1327909

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Citations (3)

Cell-attached current-clamp recordings from cortical neurons

HAL (Le Centre pour la Communication Scientifique Directe) (2020)

Azat Nasretdinov Alina Vazetdinova Fliza Valiullina-Rakhmatullina Aleksandr I. Evstifeev Roustem Khazipov

Cortical neurons

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Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

bioRxiv (Cold Spring Harbor Laboratory) (2023)

Julia Lebedeva David Jappy Azat Nasretdinov Alina Vazetdinova Viktoria Krut

Abstract For over half a century, it has been postulated that the internal excitatory circuit in the hippocampus consists of three relay stations. Excitation arrives from the entorhinal cortex to the DG granule cells, is transmitted through the mossy fibers to CA3 pyramidal cells, and is then transmitted through Schaffer collaterals to CA1 pyramidal neurons. In all three structures (DG, CA3 and CA1), the activity of the excitatory neurons involved in the synaptic transmission of excitation are under the control of inhibitory basket neurons that are recruited into network activity via feed-forward and feed-back excitation. However, in the late 90s “stratum radiatum giant cells” were described as a novel type of neuron with the anatomical features of excitatory cells. Since then, the role of these cells in the hippocampal circuitry has not been well understood. Here, using optogenetic and electrophysiological techniques we characterized the functional location of these neurons within the hippocampal network. We show that: (i) the main excitatory drive to giant excitatory neurons in stratum radiatum (ExN R ) comes via Schaffer collaterals; (ii) within the CA1 field, ExN R are not directly connected with local pyramidal cells, but provide massive and efficient excitatory input to parvalbumin positive (PV+) interneurons; (iii) ExN R are reciprocally innervated by bistratified cells, but not inhibited by backet interneurons; (iv) the efficiency of ExN R excitation to PV+ interneurons is sufficient for a single ExN R action potential to trigger massive inhibition of downstream CA1 pyramidal cells. Taken together, our data shows that ExN R constitute an alternative pathway of excitation for CA1 interneurons that avoids the burden of perisomatic inhibition.

Entorhinal cortex

Interneuron

10.1101/2023.11.20.567832

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Lactate Attenuates Synaptic Transmission and Affects Brain Rhythms Featuring High Energy Expenditure

iScience (2020)

Jan‐Oliver Hollnagel Tiziana Cesetti Justus Schneider Alina Vazetdinova Fliza Valiullina-Rakhmatullina

Lactate shuttled from blood, astrocytes, and/or oligodendrocytes may serve as the major glucose alternative in brain energy metabolism. However, its effectiveness in fueling neuronal information processing underlying complex cortex functions like perception and memory is unclear. We show that sole lactate disturbs electrical gamma and theta-gamma oscillations in hippocampal networks by either attenuation or neural bursts. Bursting is suppressed by elevating the glucose fraction in substrate supply. By contrast, lactate does not affect electrical sharp wave-ripple activity featuring lower energy use. Lactate increases the oxygen consumption during the network states, reflecting enhanced oxidative ATP synthesis in mitochondria. Finally, lactate attenuates synaptic transmission in excitatory pyramidal cells and fast-spiking, inhibitory interneurons by reduced neurotransmitter release from presynaptic terminals, whereas action potential generation in the axon is regular. In conclusion, sole lactate is less effective and potentially harmful during gamma-band rhythms by omitting obligatory ATP delivery through fast glycolysis at the synapse.

Bursting

10.1016/j.isci.2020.101316

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Citations (44)