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1

New approach for studying lamina X neurons of the spinal cord

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Krotov V., Tokhtamysh A., Dromaretskii A., Sheremet E., Belan P., Voitenko N.
Acta Neurobiologiae Experimentalis
|
2017
|
tom 77
|
nr Suppl.1
INTRODUCTION: The area around the central canal (or lamina X) is the most enigmatic lamina of the spinal cord. It is established that somatosensory integration, visceral nociception, autonomic regulation and modulation of motoneuron output are mediated by lamina X neurons, nevertheless their electrophysiological properties and functional connectivity are largely unknown. AIM(S): Electrophysiological investigations of lamina X neurons are hampered primarily by technical challenges in the preparation procedures, so we aimed to develop a reliable technique for functional studies of the neurons around the central canal. METHOD(S): Our approach relies on the method of oblique LED illumination for cell visualization in thick blocks of tissue, developed by Prof. Safronov and colleagues. RESULTS: We have developed simple, fast (5–10 min) and reliable lamina X preparation technique, that preserves whole spinal cord architecture including dorsal and ventral roots. In combination with oblique LED illumination, allowing cell visualization in thick blocks of tissue, our preparation enables visually guided patch clamp of lamina X neurons coupled with simultaneous stimulation of either afferent or efferent fibers with suction electrode. Our preparation also permits the usage of fluorescent approaches which might additionally boost the relevance of lamina X studies. First, injections of retrograde dye Fluorogold (or its analogues) into the peritoneum or lateral thalamus selectively label sympathetic preganglionic or projection neurons respectively, giving the possibility to work with these specific neuronal populations. Second, calcium transients might be recorded after loading the cells with either cell-impermeable (through the patch pipette) or cell-permeable (AM ester) Fura 2 calcium dye. CONCLUSIONS: We introduce a new methodology that combines electrophysiological and fluorescent approaches for the research of lamina X neuron functioning in physiological and pathological conditions. FINANCIAL SUPPORT: Supported by IBRO.
2

Hippocalcin signaling in spines of hippocampal neurons

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Cherkas W., Dovgan A., Fitzgerald D., Tepikin A., Borgoyne R., Belan P.
Acta Neurobiologiae Experimentalis
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2009
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tom 69
|
nr 3
Hippocalcin (HPCA) is a Ca2+-binding protein, and its Ca2+-dependent activation in hippocampal neurons is one of the necessary steps involved in many signal transduction mechanisms. In this work we have examined if synaptic glutamate receptor activation can result in HPCA signaling in spines of hippocampal neurons. Spontaneous and evoked synaptic activity induced excitatory postsynaptic potentials (EPSPs) in the hippocampal neurons leading to AP bursts and HPCA-YFP translocation to many sites in a neuronal dendritic tree including dendritic spines. In neurons clamped at −40 mV, episodes of presynaptic activity resulted in EPSCs associated with HPCA translocation mainly to dendritic spines while no translocation was observed at −70 mV . These results indicate that synaptic NMDAR activation is necessary for HPCA-YFP translocation. T- and R- rather than L-types of voltage activated Ca2+ channels also contribute to the observed translocation. FRET measurements between HPCA tagged by Yellow and Cyan Fluorescent Proteins have shown that the translocation was due to HPCA-FPs insertion in patches of spine membrane resulting in decrease of protein concentration in the cytosol of spines and diffusion of new HPCAFP molecules from the dendritic trunk. Thus, we have shown that hippocalcin may signal as a coincident detector in spines of hippocampal neurons by means of its robust insertion in spine plasma membrane.
3

The extrasynaptic AMPA receptors functioning is altered under inflammatory pain

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Kopach O., Park J., Petralia R., Sotnik A., Belan P., Tao Y., Voitenko N.
Acta Neurobiologiae Experimentalis
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2009
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tom 69
|
nr 3
We have recently shown that synaptic Ca2+-impearmable AMPA receptors (AMPARs) internalization in dorsal horn neurons underlies the maintenance of nociceptive hypersensitivity in infl ammatory pain. Here we have analyzed if traffi cking of extrasynaptic AMPARs is also changed during development and maintenance of persistent pain. We report that Complete Freund’s Adjuvant (CFA)-induced infl ammation causes an increase in functional expression of extrasynaptic AMPARs in rat substantia gelatinosa (SG) neurons during the maintenance rather than development of persistent pain. This increase, revealed as a signifi cant enhancement of AMPA-induced membrane currents and [Ca2+]i transients, was observed only in neurons characterized by an intrinsic tonic fi ring properties whereas no changes were observed in neurons exhibiting a strong adaptation. The increase was also accompanied by an enhancement of surface GluR1 expression and of the total amount of cobalt-positive neurons indicating an increase in a pool of GluR2-lacking AMPARs in extrasynaptic plasma membrane. These results suggest that functional changes in extrasynaptic AMPARs of tonic SG neurons that are associated with the maintenance of nociceptive hypersensitivity may also contribute to infl ammatory pain. We also suppose that there is a different contribution of tonic and transient neurons to the detection of peripheral painful stimuli and to maintenance of nociceptive hypersensitivity.
4

Subpopulation of c-fiber-activated lamina I projection neurons with unique input-output characteristics for the nmdar-dependent nociceptive coding

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Agashkov K., Krotov V., Krasniakova M., Shevchuk D., Liashenko A., Safronov B., Voitenko N., Belan P.
Acta Neurobiologiae Experimentalis
|
2017
|
tom 77
|
nr Suppl.1
INTRODUCTION: Spinal lamina I projection neurons (PNs) are key elements of the pain processing system, which relay peripheral input to supraspinal structures generating sensation of pain. The population of PNs is small (~5% of lamina I neurons) but very heterogeneous according to their intrinsic and synaptic properties. AIM(S): Investigate mechanisms of acute nociception encoding and evaluate input-output characteristics of lamina I PNs. METHOD(S): Whole-cell recordings from lamina I PNs retrogradely-labeled via the lateral PB area in an intact spinal cord preparation with attached dorsal roots. RESULTS: We identified a specific group of PNs (16%) with unique properties. In these PNs (SB-PNs), a stimulation of nociceptive afferents evoked gradual strength‑dependent amplification of afferent input expressed as an increase in the number of generated APs. Upon a root stimulation at C‑fiber‑intensity, the SB‑PN group generated more than 80% of spikes of the entire population of PNs, thus, being the major group of PNs codifying acute pain sensation. We have also identified several mechanisms of this nociceptive input amplification. First, SB‑PNs are intensively innervated by the high‑threshold A delta‑ and C‑afferents providing robust and reliable spike generation. Second, the nociceptive input was amplified by intrinsic bursting capabilities of SB PNs. Third, the afferent input was prolonged (to 0.-1.5 s) and potentiated (to -45 mV to -20 mV) by the NMDAR-dependent synaptic component forming intrinsic plateau potentials generated by SB‑PNs. The afferent stimulation increased, for several seconds, spontaneous excitatory drive to SB-PNs that became suprathreshold and evoked series of spikes. CONCLUSIONS: We have described a new type of lamina I PNs efficiently transmitting the main part of primary nociceptive input to supraspinal structures playing an important role in acute pain generation. A complex interplay between synaptic, intrinsic and network activities underlies unique nociceptive encoding features of this group of PNs. FINANCIAL SUPPORT: Supported by IBRO.
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