Neurotrophin‐dependent plasticity of neurotransmitter segregation in the rat superior cervical ganglion <i>in vivo</i>

Vega, Alberto; Cancino-Rodezno, Angeles; Valle-Leija, Pablo; Sánchez-Tafolla, Berardo M.; Elinos, Diana; Cifuentes, Fredi; Morales, M.A.

doi:10.1002/dneu.22362

Cited by 9 publications

(9 citation statements)

References 74 publications

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“…Thus, addition of ciliary neurotrophic factor (CNTF) increases the degree of segregation of NE and NPY in varicosities of sympathetic ganglionic neurons co-cultured with cardiomyocytes (Vega et al, 2010 ). Furthermore, the neurotrophin, nerve growth factor (NGF) changes the segregation of ACh and methionine-enkephalin (mENK) in preganglionic sympathetic neuronal varicosities in vivo (Vega et al, 2016 ). Considering these evidences, we explored whether plastic changes in the segregation of neurotransmitters can also occur in physio-pathologic conditions, like stress and hypertension, conditions that course with augmented sympathetic activity.…”

Section: Discussionmentioning

confidence: 99%

“…However, later evidence showed that neurons are able to segregate their neurotransmitters, and independently store and release them at distinct terminals, allowing neurons to exert each transmitter function separately (Fisher et al, 1988 ; Hattori et al, 1991 ; Morales et al, 1995 ; Sámano et al, 2012 ; Zhang et al, 2015 ). Like other neurons, sympathetic ones have this capability to segregate their neurotransmitters (Morales et al, 1995 ; Chanthaphavong et al, 2003 ; Sámano et al, 2006 , 2009 ; Vega et al, 2010 , 2016 ).…”

Section: Introductionmentioning

confidence: 99%

“…Neurotransmitter segregation is a plastic phenomenon that depends on neuronal requirements (Sámano et al, 2012 ). For instance, we demonstrated that in rat sympathetic neurons, both in vitro and in vivo , neurotransmitter segregation is modulated by neurotrophic factors (Vega et al, 2010 , 2016 ). Additionally, we found a likely functional role of segregation in the rat superior cervical ganglia (SCG), we detected a correlation between the level of segregation of ACh and GABA, and the strength of synaptic transmission, where more segregation correlates with stronger synaptic transmission (Elinos et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

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Sympathetic Hyperactivity and Age Affect Segregation and Expression of Neurotransmitters

Merino-Jiménez

Miguel

Pliego

et al. 2018

Front. Cell. Neurosci.

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Sympathetic neurons of the rat superior cervical ganglion (SCG) can segregate their neurotransmitters and co-transmitters to separate varicosities of single axons. We have shown that transmitter segregation is a plastic phenomenon and that it is correlated with the strength of synaptic transmission. Here, we determined whether sympathetic dysfunction occurring in stress and hypertension was correlated with plastic changes of neurotransmitter segregation. We characterized the expression of the markers, L-glutamic acid decarboxylase of 67 kDa (GAD67) and vesicular acetylcholine (ACh) transporter (VAChT) in the SCG of cold stressed and spontaneously hypertensive rats (SHR). Considering that the SCG comprises a heterogeneous neuronal population, we explored whether the expression and segregation of neurotransmitters would also have an intraganglionic heterogeneous distribution in ganglia of stressed and hypertensive rats. Furthermore, since hypertension in SHR is detected around 8–10 weeks, we evaluated expression and segregation of ACh and GABA in adult hypertensive (12-week old (wo)) and young pre-hypertensive (6-wo) SHR. We found an increase in segregation of ACh and GABA with no change in transmitter expression in ganglia of stressed animals. In contrast, in SHR, there was an increase in GABA expression, although segregation did not vary. Segregation showed a caudo-rostral gradient in controls but not in the ganglia of stressed animals. GABA expression showed a rostro-caudal gradient in adult SHR, which was not present in young 6-wo rats. In young SHR, ACh increased and, unexpectedly, segregation of ACh and GABA was higher than in adults. Data suggest that ACh and GABA segregation increases in acute sympathetic hyperactivity like stress, but does not vary in chronic hyperactivity such as in hypertension. Changes in segregation are age-dependent and might be involved in the mechanisms underlying stress and hypertension.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Sympathetic Hyperactivity and Age Affect Segregation and Expression of Neurotransmitters

Merino-Jiménez

Miguel

Pliego

et al. 2018

Front. Cell. Neurosci.

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“…Gärtner and Staiger (2002) demonstrated that short high-frequency bursts of stimuli that induce LTP also evoke the instantaneous secretion of BDNF in primary cultures of hippocampal neurons. The fact that BDNF and NGF are expressed in the neurons of the SCG in adult rats (Wetmore and Olson, 1995; Vega et al, 2016) supports this possibility.…”

Section: Discussionmentioning

confidence: 96%

Presence of Functional Neurotrophin TrkB Receptors in the Rat Superior Cervical Ganglion

et al. 2017

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Sympathetic neurons express the neurotrophin receptors TrkA, p75NTR, and a non-functional truncated TrkB isoform (TrkB-Tc), but are not thought to express a functional full-length TrkB receptor (TrkB-Fl). We, and others, have demonstrated that nerve growth factor (NGF) and brain derived neurotrophic factor (BDNF) modulate synaptic transmission and synaptic plasticity in neurons of the superior cervical ganglion (SCG) of the rat. To clarify whether TrkB is expressed in sympathetic ganglia and contributes to the effects of BDNF upon sympathetic function, we characterized the presence and activity of the neurotrophin receptors expressed in the adult SCG compared with their presence in neonatal and cultured sympathetic neurons. Here, we expand our previous study regarding the immunodetection of neurotrophin receptors. Immunohistochemical analysis revealed that 19% of adult ganglionic neurons expressed TrkB-Fl immunoreactivity (IR), 82% expressed TrkA-IR, and 51% expressed p75NTR-IR; TrkB-Tc would be expressed in 36% of neurons. In addition, using Western-blotting and reverse transcriptase polymerase chain reaction (RT-PCR) analyses, we confirmed the expression of TrkB-Fl and TrkB-Tc protein and mRNA transcripts in adult SCG. Neonatal neurons expressed significantly more TrkA-IR and TrkB-Fl-IR than p75NTR-IR. Finally, the application of neurotrophin, and high frequency stimulation, induced the activation of Trk receptors and the downstream PI3-kinase (phosphatidyl inositol-3-kinase) signaling pathway, thus evoking the phosphorylation of Trk and Akt. These results demonstrate that SCG neurons express functional TrkA and TrkB-Fl receptors, which may contribute to the differential modulation of synaptic transmission and long-term synaptic plasticity.

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“…Segregation between ACh and m-Enk can be modified by endogenous neurotrophic factors in the SPN in vivo. We showed that axotomy produces a decrease in endogenous nerve growth factor (NGF) content and an enhancement of ACh and m-Enk segregation in the rat SCG; these effects were counteracted by NGF administration ( Vega et al, 2016 ; Figure 1 ). Considering these findings, we wondered whether neurotransmitter segregation varies in different physiopathological conditions, such as stress and hypertension.…”

Section: Neurotransmitter Segregation Plasticitymentioning

confidence: 99%

Functional Implications of Neurotransmitter Segregation

Cifuentes

Morales

2021

Front. Neural Circuits

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Here, we present and discuss the characteristics and properties of neurotransmitter segregation, a subtype of neurotransmitter cotransmission. We review early evidence of segregation and discuss its properties, such as plasticity, while placing special emphasis on its probable functional implications, either in the central nervous system (CNS) or the autonomic nervous system. Neurotransmitter segregation is a process by which neurons separately route transmitters to independent and distant or to neighboring neuronal processes; it is a plastic phenomenon that changes according to synaptic transmission requirements and is regulated by target-derived signals. Distant neurotransmitter segregation in the CNS has been shown to be related to an autocrine/paracrine function of some neurotransmitters. In retinal amacrine cells, segregation of acetylcholine (ACh) and GABA, and glycine and glutamate to neighboring terminals has been related to the regulation of the firing rate of direction-selective ganglion cells. In the rat superior cervical ganglion, segregation of ACh and GABA to neighboring varicosities shows a heterogeneous regional distribution, which is correlated to a similar regional distribution in transmission strength. We propose that greater segregation of ACh and GABA produces less GABAergic inhibition, strengthening ganglionic transmission. Segregation of ACh and GABA varies in different physiopathological conditions; specifically, segregation increases in acute sympathetic hyperactivity that occurs in cold stress, does not vary in chronic hyperactivity that occurs in hypertension, and rises in early ages of normotensive and hypertensive rats. Given this, we propose that variations in the extent of transmitter segregation may contribute to the alteration of neural activity that occurs in some physiopathological conditions and with age.

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Neurotrophin‐dependent plasticity of neurotransmitter segregation in the rat superior cervical ganglion in vivo

Cited by 9 publications

References 74 publications

Sympathetic Hyperactivity and Age Affect Segregation and Expression of Neurotransmitters

Sympathetic Hyperactivity and Age Affect Segregation and Expression of Neurotransmitters

Presence of Functional Neurotrophin TrkB Receptors in the Rat Superior Cervical Ganglion

Functional Implications of Neurotransmitter Segregation

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