On the role of volume transmission and receptor–receptor interactions in social behaviour: Focus on central catecholamine and oxytocin neurons

Fuxé, Kjell; Borroto‐Escuela, Dasiel O.; Romero-Fernández, Wilber; Ciruela, Francisco; Manger, Paul P.R.; Leo, Giuseppina; Dı́az-Cabiale, Zaida; Agnati, Luigi F.

doi:10.1016/j.brainres.2012.01.062

Cited by 71 publications

(62 citation statements)

References 80 publications

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“…To attempt to reduce network complexity, one common approach is to define network subunits and demonstrate their functional role by selective removal. It is well known that amine neurons can signal through hormonal volume transmission and act on targets at a distance [52], [53]. However, biogenic amines are also released synaptically and act on local targets [54]–[58].…”

Section: Discussionmentioning

confidence: 99%

Octopamine Neuromodulation Regulates Gr32a-Linked Aggression and Courtship Pathways in Drosophila Males

Andrews

Fernández

et al. 2014

PLoS Genet

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Chemosensory pheromonal information regulates aggression and reproduction in many species, but how pheromonal signals are transduced to reliably produce behavior is not well understood. Here we demonstrate that the pheromonal signals detected by Gr32a-expressing chemosensory neurons to enhance male aggression are filtered through octopamine (OA, invertebrate equivalent of norepinephrine) neurons. Using behavioral assays, we find males lacking both octopamine and Gr32a gustatory receptors exhibit parallel delays in the onset of aggression and reductions in aggression. Physiological and anatomical experiments identify Gr32a to octopamine neuron synaptic and functional connections in the suboesophageal ganglion. Refining the Gr32a-expressing population indicates that mouth Gr32a neurons promote male aggression and form synaptic contacts with OA neurons. By restricting the monoamine neuron target population, we show that three previously identified OA-FruM neurons involved in behavioral choice are among the Gr32a-OA connections. Our findings demonstrate that octopaminergic neuromodulatory neurons function as early as a second-order step in this chemosensory-driven male social behavior pathway.

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Section: Discussionmentioning

confidence: 99%

Octopamine Neuromodulation Regulates Gr32a-Linked Aggression and Courtship Pathways in Drosophila Males

Andrews

Fernández

et al. 2014

PLoS Genet

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“…There are two morphologically distinct classes of serotonergic axons (Kosofsky and Molliver, 1987): beaded axons with large, spherical varicosities (up to 5 µm in diameter), which make synaptic contact with their targets (so-called M-fibers, Törk, 1990), and fine axons with small (smaller than 1 µm in diameter) varicosities (the main fibers, ubiquitous throughout the mammalian cerebral cortex and also called D-fibers, Törk, 1990), which lack membrane junctional complexes (synapse) and release serotonin diffusely through volume transmission (Törk, 1990; Descarries et al, 1991; Descarries and Mechawar, 2000; De-Miguel and Trueta, 2005; Fuxe et al, 2012). The third and least common type was first described in the marmoset, and is thought to be the stem fibers for M-fibers (Hornung et al, 1990).…”

Section: Chemical Neuroanatomy Of the Monoaminergic Systemsmentioning

confidence: 99%

Monoaminergic neuropathology in Alzheimer’s disease

Šimić

Leko

Wray³

et al. 2017

Progress in Neurobiology

223

142

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None of the proposed mechanisms of Alzheimer’s disease (AD) fully explains the distribution patterns of the neuropathological changes at the cellular and regional levels, and their clinical correlates. One aspect of this problem lies in the complex genetic, epigenetic, and environmental landscape of AD: early-onset AD is often familial with autosomal dominant inheritance, while the vast majority of AD cases are late-onset, with the ε4 variant of the gene encoding apolipoprotein E (APOE) known to confer a 5–20 fold increased risk with partial penetrance. Mechanisms by which genetic variants and environmental factors influence the development of AD pathological changes, especially neurofibrillary degeneration, are not yet known. Here we review current knowledge of the involvement of the monoaminergic systems in AD. The changes in the serotonergic, noradrenergic, dopaminergic, histaminergic, and melatonergic systems in AD are briefly described. We also summarize the possibilities for monoamine-based treatment in AD. Besides neuropathologic AD criteria that include the noradrenergic locus coeruleus (LC), special emphasis is given to the serotonergic dorsal raphe nucleus (DRN). Both of these brainstem nuclei are among the first to be affected by tau protein abnormalities in the course of sporadic AD, causing behavioral and cognitive symptoms of variable severity. The possibility that most of the tangle-bearing neurons of the LC and DRN may release amyloid β as well as soluble monomeric or oligomeric tau protein trans-synaptically by their diffuse projections to the cerebral cortex emphasizes their selective vulnerability and warrants further investigations of the monoaminergic systems in AD.

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“…Thus, increased short distance (micro range) extrasynaptic VT of the classical synaptic transmitters glutamate and GABA develop with reductions in the astroglial barrier. The targets were both glial and neuronal cells with receptors and transporters for glutamate and GABA [16][17][18]28]. Recently, surface diffusion of astrocytic glutamate transporters were found to shape the kinetics of excitatory postsynaptic currents and thus synaptic transmission [32].…”

Section: Comparison Between Soluble and Extracellular Vesicle-mediatementioning

confidence: 99%

The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural–glial networks

Borroto-Escuela

Agnati

Bechter

et al. 2015

Phil. Trans. R. Soc. B

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110

130

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One contribution of 16 to a discussion meeting issue 'Release of chemical transmitters from cell bodies and dendrites of nerve cells'. Two major types of intercellular communication are found in the central nervous system (CNS), namely wiring transmission (point-to-point communication, the prototype being synaptic transmission with axons and terminals) and volume transmission (VT; communication in the extracellular fluid and in the cerebrospinal fluid (CSF)) involving large numbers of cells in the CNS. Volume and synaptic transmission become integrated inter alia through the ability of their chemical signals to activate different types of receptor protomers in heteroreceptor complexes located synaptically or extrasynaptically in the plasma membrane. The demonstration of extracellular dopamine (DA) and serotonin (5-HT) fluorescence around the DA and 5-HT nerve cell bodies with the Falck-Hillarp formaldehyde fluorescence method after treatment with amphetamine and chlorimipramine, respectively, gave the first indications of the existence of VT in the brain, at least at the soma level. There exist different forms of VT. Early studies on VT only involved spread including diffusion and flow of soluble biological signals, especially transmitters and modulators, a communication called extrasynaptic (short distance) and long distance (paraaxonal and paravascular and CSF pathways) VT. Also, the extracellular vesicle type of VT was demonstrated. The exosomes (endosome-derived vesicles) appear to be the major vesicular carriers for VT but the larger microvesicles also participate. Both mainly originate at the soma-dendritic level. They can transfer lipids and proteins, including receptors, Rab GTPases, tetraspanins, cholesterol, sphingolipids and ceramide. Within them there are also subsets of mRNAs and non-coding regulatory microRNAs. At the soma-dendritic membrane, sets of dynamic postsynaptic heteroreceptor complexes (built up of different types of physically interacting receptors and proteins) involving inter alia G protein-coupled receptors including autoreceptors, ion channel receptors and receptor tyrosine kinases are hypothesized to be the molecular basis for learning and memory. At nerve terminals, the presynaptic heteroreceptor complexes are postulated to undergo plastic changes to maintain the pattern of multiple transmitter release reflecting the firing pattern to be learned by the heteroreceptor complexes in the postsynaptic membrane.

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On the role of volume transmission and receptor–receptor interactions in social behaviour: Focus on central catecholamine and oxytocin neurons

Cited by 71 publications

References 80 publications

Octopamine Neuromodulation Regulates Gr32a-Linked Aggression and Courtship Pathways in Drosophila Males

Octopamine Neuromodulation Regulates Gr32a-Linked Aggression and Courtship Pathways in Drosophila Males

Monoaminergic neuropathology in Alzheimer’s disease

The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural–glial networks

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