Organization of efferent peripheral synapses at mechanosensory neurons in spiders

Fabian-Fine, Ruth; Meinertzhagen, Ian A.; Seyfarth, Ernst‐August

doi:10.1002/(sici)1096-9861(20000501)420:2<195::aid-cne4>3.0.co;2-q

Cited by 26 publications

(43 citation statements)

References 57 publications

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“…23 nm in diameter) electron lucent vesicles whereas glutamatergic synapses are characterized by large (approx. 41 nm in diameter) electron lucent vesicles (Fabian-Fine et al 2000). These vesicle profiles confirm our light microscopic observations of numerous morphologically distinguishable GABA-and glutamate-IR axons along muscle fibers, and the fact that these indeed form synaptic contacts onto those fibers.…”

Section: Discussionsupporting

confidence: 86%

“…We anticipated that these neurons would form synaptic contacts onto muscle fibers and reveal the same type of immunolabeling in their axon terminals as they show in their somata. We would furthermore expect to see a diversity of presynaptic profiles at the ultrastructural level, given that different types of vesicles are thought to contain different neurotransmitters (Peters and Palay 1996;Fabian-Fine et al 2000;de Camilli et al 2001;Torrealba and Carrasco 2004). We examined muscle tissue in the spider patella at both LMand EM-levels to address these questions.…”

Section: Anti-vesicular Gaba Transporter Immunolabelingmentioning

confidence: 99%

“…Serial-section electron microscopic investigations of peripheral synaptic contacts have shown various forms of presumed efferent contacts onto sensory neurons, with surrounding glia, and between putative efferent fibers themselves (Fabian-Fine et al 2000). Some synaptic profiles contain a mixed population of synaptic vesicles, suggesting that the neurons co-release different neurotransmitters (Fabian-Fine et al 2000).…”

Section: Introductionmentioning

confidence: 99%

“…Some synaptic profiles contain a mixed population of synaptic vesicles, suggesting that the neurons co-release different neurotransmitters (Fabian-Fine et al 2000). Evidence for the co-expression of two or more classical neurotransmitters has accumulated in recent years (Dal Bo et al 2004; Barreiro-Iglesias et al 2009;Chuhma et al 2009;Liu et al 2013).…”

Section: Introductionmentioning

confidence: 99%

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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: Discussionsupporting

confidence: 86%

Section: Anti-vesicular Gaba Transporter Immunolabelingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2015

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“…In the tropical wandering spider Cupiennius salei, many of the efferent fibers are GABAergic (Fabian-Fine et al, 1999b), and the mechanosensory neurons are modulated by GABA acting on both ionotropic and metabotropic GABA receptors (Panek et al, 2002(Panek et al, , 2003. The large variety of synaptic contacts between the efferent fibers and sensory neurons, between the efferent fibers and glial cells, and between the efferent neurons themselves (Fabian-Fine et al, 2000) suggest that other transmitters also affect these mechanosensilla. Octopamine is a probable candidate, because octopamine-immunoreactive neurons were previously found in the C. salei CNS and free octopamine was detected in its hemolymph (Seyfarth et al, 1993).…”

Section: Introductionmentioning

confidence: 99%

Spider Peripheral Mechanosensory Neurons Are Directly Innervated and Modulated by Octopaminergic Efferents

Widmer

Höger²,

Meisner³

et al. 2005

J. Neurosci.

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Octopamine is a chemical relative of noradrenaline providing analogous neurohumoral control of diverse invertebrate physiological processes. There is also evidence for direct octopaminergic innervation of some insect peripheral tissues. Here, we show that spider peripheral mechanoreceptors are innervated by octopamine-containing efferents. The mechanosensory neurons have octopamine receptors colocalized with synapsin labeling in the efferent fibers. In addition, octopamine enhances the electrical response of the sensory neurons to mechanical stimulation.Spider peripheral mechanosensilla receive extensive efferent innervation. Many efferent fibers in the legs of Cupiennius salei are GABAergic, providing inhibitory control of sensory neurons, but there is also evidence for other neurotransmitters. We used antibody labeling to show that some efferents contain octopamine and that octopamine receptors are concentrated on the axon hillocks and proximal soma regions of all mechanosensory neurons in the spider leg. Synaptic vesicles in efferent neurons were concentrated in similar areas.Octopamine, or its precursor tyramine, increased responses of mechanically stimulated filiform (trichobothria) leg hairs. This effect was blocked by the octopamine antagonist phentolamine. The octopamine-induced modulation was mimicked by 8-Br-cAMP, a cAMP analog, and blocked by Rp-cAMPS, a protein kinase A inhibitor, indicating that spider octopamine receptors activate adenylate cyclase and increase cAMP concentration.Frequency response analysis showed that octopamine increased the sensitivity of the trichobothria neurons over a broad frequency range. Thus, the major effect of octopamine is to increase its overall sensitivity to wind-borne signals from sources such as flying insect prey or predators.

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Tyrosine hydroxylase immunolabeling reveals the distribution of catecholaminergic neurons in the central nervous systems of the spiders Hogna lenta (Araneae: Lycosidae) and Phidippus regius (Araneae: Salticidae)

Auletta

Rue

Harley

et al. 2019

J of Comparative Neurology

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With over 48,000 species currently described, spiders (Arthropoda: Chelicerata: Araneae) comprise one of the most diverse groups of animals on our planet, and exhibit an equally wide array of fascinating behaviors. Studies of central nervous systems (CNSs) in spiders, however, are relatively sparse, and no reports have yet characterized catecholaminergic (dopamine [DA]‐ or norepinephrine‐synthesizing) neurons in any spider species. Because these neuromodulators are especially important for sensory and motor processing across animal taxa, we embarked on a study to identify catecholaminergic neurons in the CNS of the wolf spider Hogna lenta (Lycosidae) and the jumping spider Phidippus regius (Salticidae). These neurons were most effectively labeled with an antiserum raised against tyrosine hydroxylase (TH), the rate‐limiting enzyme in catecholamine synthesis. We found extensive catecholamine‐rich neuronal fibers in the first‐ and second‐order optic neuropils of the supraesophageal mass (brain), as well as in the arcuate body, a region of the brain thought to receive visual input and which may be involved in higher order sensorimotor integration. This structure likely shares evolutionary origins with the DA‐enriched central complex of the Mandibulata. In the subesophageal mass, we detected an extensive filigree of TH‐immunoreactive (TH‐ir) arborizations in the appendage neuromeres, as well as three prominent plurisegmental fiber tracts. A vast abundance of TH‐ir somata were located in the opisthosomal neuromeres, the largest of which appeared to project to the brain and decorate the appendage neuromeres. Our study underscores the important roles that the catecholamines likely play in modulating spider vision, higher order sensorimotor processing, and motor patterning.

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Organization of efferent peripheral synapses at mechanosensory neurons in spiders

Cited by 26 publications

References 57 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

Spider Peripheral Mechanosensory Neurons Are Directly Innervated and Modulated by Octopaminergic Efferents

Tyrosine hydroxylase immunolabeling reveals the distribution of catecholaminergic neurons in the central nervous systems of the spiders Hogna lenta (Araneae: Lycosidae) and Phidippus regius (Araneae: Salticidae)

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