Dual-transmitter neurons: functional implications of co-release and co-transmission

Vaaga, Christopher E.; Borisovska, Maria; Westbrook, Gary L.

doi:10.1016/j.conb.2014.04.010

Cited by 165 publications

(144 citation statements)

References 89 publications

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“…Co-transmission of neurotransmitters has received increasing attention recently (Seal and Edwards 2006;Vaaga et al 2014). Glutamate is the main excitatory neurotransmitter at neuromuscular junctions in Drosophila (Jan and Jan 1976) and both immunocytochemical and electrophysiological studies have demonstrated that glutamate may also be released at peripheral synapses in the spider nervous system (Fabian-Fine et al 1999b;Panek and Torkkeli 2005).…”

Section: Anti-vesicular Gaba Transporter Immunolabelingmentioning

confidence: 99%

Co-localization of Gamma-Aminobutyric Acid and Glutamate in Neurons of the Spider Central Nervous System

et al. 2015

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Spider sensory neurons with cell bodies close to various sensory organs are innervated by putative efferent axons from the central nervous system (CNS). Light and electronmicroscopic imaging of immunolabeled neurons has demonstrated that neurotransmitters present at peripheral synapses include γ-aminobutyric acid (GABA), glutamate and octopamine. Moreover, electrophysiological studies show that these neurotransmitters modulate the sensitivity of peripheral sensory neurons. Here, we undertook immunocytochemical investigations to characterize GABA and glutamate-immunoreactive neurons in three-dimensional reconstructions of the spider CNS. We document that both neurotransmitters are abundant in morphologically distinct neurons throughout the CNS. Labeling for the vesicular transporters, VGAT for GABA and VGLUT for glutamate, showed corresponding patterns, supporting the specificity of antibody binding. Whereas some neurons displayed strong immunolabeling, others were only weakly labeled. Double labeling showed that a subpopulation of weakly labeled neurons present in all ganglia expresses both GABA and glutamate. Double labeled, strongly and weakly labeled GABA and glutamate immunoreactive axons were also observed in the periphery along muscle fibers and peripheral sensory neurons. Electron microscopic investigations showed presynaptic profiles of various diameters with mixed vesicle populations innervating muscle tissue as well as sensory neurons. Our findings provide evidence that: (1) sensory neurons and muscle fibers are innervated by morphologically distinct, centrally located GABA- and glutamate immunoreactive neurons; (2) a subpopulation of these neurons may co-release both neurotransmitters; and (3) sensory neurons and muscles are innervated by all of these neurochemically and morphologically distinct types of neurons. The biochemical diversity of presynaptic innervation may contribute to how spiders filter natural stimuli and coordinate appropriate response patterns.

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Section: Anti-vesicular Gaba Transporter Immunolabelingmentioning

confidence: 99%

Co-localization of Gamma-Aminobutyric Acid and Glutamate in Neurons of the Spider Central Nervous System

et al. 2015

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“…Neurons signal using more than one chemical transmission mechanism, including co-transmission of different classes of neurotransmitter from distinct vesicles or co-release from the same vesicle [178][179][180][181][182][183]. This has long been recognized [181,184], but modern techniques provide excellent tools to detect co-transmission/release while mapping it onto defined neurons.…”

Section: Questions Limitations and Future Directionsmentioning

confidence: 99%

Contemporary approaches to neural circuit manipulation and mapping: focus on reward and addiction

Saunders

Janak

2015

Phil. Trans. R. Soc. B

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One contribution of 15 to a theme issue 'Controlling brain activity to alter perception, behaviour and society'. Tying complex psychological processes to precisely defined neural circuits is a major goal of systems and behavioural neuroscience. This is critical for understanding adaptive behaviour, and also how neural systems are altered in states of psychopathology, such as addiction. Efforts to relate psychological processes relevant to addiction to activity within defined neural circuits have been complicated by neural heterogeneity. Recent advances in technology allow for manipulation and mapping of genetically and anatomically defined neurons, which when used in concert with sophisticated behavioural models, have the potential to provide great insight into neural circuit bases of behaviour. Here we discuss contemporary approaches for understanding reward and addiction, with a focus on midbrain dopamine and cortico-striato-pallidal circuits.

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“…The ability to optogenetically activate genetically-defined cell types has led to a growing appreciation that mammalian neurons can release multiple fast-acting neurotransmitters (Hnasko and Edwards, 2012; Vaaga et al, 2014), subverting the classic notion that neuron classes can be defined by their ability to package and release a single primary neurotransmitter. Examples include spinal interneurons that release GABA and glycine (Jonas et al, 1998), midbrain dopaminergic neurons that also release glutamate and/or GABA (Stuber et al, 2010; Tecuapetla et al, 2010; Tritsch et al, 2012, 2014), and habenula-projecting neurons that release both GABA and glutamate (Root et al, 2014; Shabel et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Cotransmission of acetylcholine and GABA

et al. 2016

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Neurons that produce acetylcholine (ACh) are positioned to broadly influence the brain, with axonal arborizations that extend throughout the cerebral cortex, striatum, and hippocampus. While the action of these neurons has typically been attributed entirely to ACh, neurons often release more than one primary neurotransmitter. Here, we review evidence for the cotransmission of the inhibitory neurotransmitter GABA from cholinergic neurons throughout the mammalian central nervous system. Functional cotransmission of ACh and GABA has been reported in the retina and cortex, and anatomical studies suggest that GABA cotransmission is a common feature of nearly all forebrain ACh-producing neurons. Further experiments are necessary to confirm the extent of GABA cotransmission from cholinergic neurons, and the contribution of GABA needs to be considered when studying the functional impact of activity in ACh-producing neurons.

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Dual-transmitter neurons: functional implications of co-release and co-transmission

Cited by 165 publications

References 89 publications

Co-localization of Gamma-Aminobutyric Acid and Glutamate in Neurons of the Spider Central Nervous System

Co-localization of Gamma-Aminobutyric Acid and Glutamate in Neurons of the Spider Central Nervous System

Contemporary approaches to neural circuit manipulation and mapping: focus on reward and addiction

Cotransmission of acetylcholine and GABA

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