Tachykinin-Related Peptide and GABA-Mediated Presynaptic Inhibition of Crayfish Photoreceptors

Glantz, Raymon M.; Miller, Clyde S.; Nässel, Dick R.

doi:10.1523/jneurosci.20-05-01780.2000

Cited by 53 publications

(48 citation statements)

References 81 publications

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“…Our preliminary data, however, suggest that the 2 compounds may act independently. This is in contrast to findings in the crayfish visual system where GABA hyperpolarizes photoreceptors and a tachykinin-like peptide potentiates this response (47). In the crayfish, it is not clear which GABA receptor type that mediates the response, although a Cl Ϫ conductance appears to be activated (47), whereas in Drosophila ORNs the presynaptic inhibition is mediated by metabotropic GABA B receptors (9).…”

Section: Discussioncontrasting

confidence: 61%

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Ignell

Root

Birse

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The role of classical neurotransmitters in the transfer and processing of olfactory information is well established in many organisms. Neuropeptide action, however, is largely unexplored in any peripheral olfactory system. A subpopulation of local interneurons (LNs) in the Drosophila antannal lobe is peptidergic, expressing Drosophila tachykinins (DTKs). We show here that olfactory receptor neurons (ORNs) express the DTK receptor (DTKR). Using twophoton microscopy, we found that DTK applied to the antennal lobe suppresses presynaptic calcium and synaptic transmission in the ORNs. Furthermore, reduction of DTKR expression in ORNs by targeted RNA interference eliminates presynaptic suppression and alters olfactory behaviors. We detect opposite behavioral phenotypes after reduction and over expression of DTKR in ORNs. Our findings suggest a presynaptic inhibitory feedback to ORNs from peptidergic LNs in the antennal lobe.olfactory behavior ͉ presynaptic inhibition ͉ tachykinin ͉ two-photon imaging I n Drosophila, odor detection begins when odor molecules activate olfactory receptor neurons (ORNs) in the antennae and maxillary palps. Each of the ORNs expresses only 1 or a few members of a large family of odorant receptor genes (1-4). These ORNs propagate activity to neurons with dendrites in the glomerular compartments of the antennal lobe; each glomerulus receives inputs from ORNs that express the same odorant receptor (1, 3, 5, 6). In the glomeruli, the activity is read by second-order neurons, designated projection neurons (PNs), which relay information to higher olfactory centers in the brain (7).Inhibitory circuits in the glomeruli, mediated by local interneurons (LNs), play a key role in modulating glomerular signal activity. Presynaptic GABAergic inhibition of the ORNs has been shown in both Drosophila (8, 9) and in mammals (10-12). Conversely, cholinergic LNs in the Drosophila antennal lobe have been suggested to increase and redistribute odor-evoked activity at low odor concentrations (13,14).In addition to GABA and acetylcholine it is likely that certain neuropeptides are used as neuromodulators in the antennal lobe circuitry of insects (15, 16), as also suggested in the olfactory bulb in mammals (17,18). One neuropeptide gene that has been implicated in olfactory processing is dtk (19), a gene encoding 5 tachykinin-related peptides, DTKs (20). The DTKs are expressed in Ϸ150 neurons in the Drosophila brain, and in the antennal lobe glomeruli, there are extensive DTK-immunoreactive arborizations derived from a subset of antennal lobe LNs (21). Two DTK receptors, DTKR and NKD, have been identified in Drosophila (22, 23) and 1 of these, DTKR, is strongly expressed in antennal lobe glomeruli (24). Behavioral evidence for a role of DTKs in olfaction was obtained from analysis of flies where dtk expression was knocked down globally using RNA interference (RNAi); these flies displayed diminished odor sensitivity (19).To gain insight into the neuromodulation provided by the DTK signaling system in the antennal lob...

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Section: Discussioncontrasting

confidence: 61%

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Ignell

Root

Birse

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

167

197

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“…Immunohistochemical studies using these antibodies have shown that CabTRP Ia is widely distributed within the nervous system of decapod crustaceans (Mancillas et al, 1981;Fingerman et al, 1985;Goldberg et al, 1988;Sandeman et al, 1990a,b;Ache, 1994, 1997;Blitz et al, 1995Blitz et al, , 1999Christie et al, 1995aChristie et al, , 1997aSchmidt, 1997a,b;Langworthy et al, 1997;Fénelon et al, 1999;Glantz et al, 2000;Thirumalai and Marder, 2002;Pulver and Marder, 2002). In C. borealis, P. interruptus and H. americanus, one area of the nervous system that exhibits TRP immunoreactivity is the stomatogastric nervous system (STNS; Fig.·1), which controls the movement of the foregut musculature (Goldberg et al, 1988;Blitz et al, 1995Blitz et al, , 1999Christie et al, 1997a,b;Fénelon et al, 1999).…”

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confidence: 99%

Identification and characterization of a tachykinin-containing neuroendocrine organ in the commissural ganglion of the crabCancer productus

Messinger

Kutz

et al. 2005

Journal of Experimental Biology

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SUMMARY A club-shaped, tachykinin-immunopositive structure first described nearly two decades ago in the commissural ganglion (CoG) of three species of decapod crustaceans has remained enigmatic, as its function is unknown. Here, we use a combination of anatomical, mass spectrometric and electrophysiological techniques to address this issue in the crab Cancer productus. Immunohistochemistry using an antibody to the vertebrate tachykinin substance P shows that a homologous site exists in each CoG of this crab. Confocal microscopy reveals that its structure and organization are similar to those of known neuroendocrine organs. Based on its location in the anterior medial quadrant of the CoG, we have named this structure the anterior commissural organ (ACO). Matrix-assisted laser desorption/ionization Fourier transform mass spectrometry shows that the ACO contains the peptide APSGFLGMRamide,commonly known as Cancer borealis tachykinin-related peptide Ia(CabTRP Ia). Using the same technique, we show that CabTRP Ia is also released into the hemolymph. As no tachykinin-like labeling is seen in any of the other known neuroendocrine sites of this species (i.e. the sinus gland, the pericardial organ and the anterior cardiac plexus), the ACO is a prime candidate to be the source of CabTRP Ia present in the circulatory system. Our electrophysiological studies indicate that one target of hemolymph-borne CabTRP Ia is the foregut musculature. Here, no direct CabTRP Ia innervation is present, yet several gastric mill and pyloric muscles are nonetheless modulated by hormonally relevant concentrations of the peptide. Collectively,our findings show that the C. productus ACO is a neuroendocrine organ providing hormonal CabTRP Ia modulation to the foregut musculature. Homologous structures in other decapods are hypothesized to function similarly.

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“…In the visual system of vertebrates and invertebrates, feedback is used to sharpen the visual field (28,29). Another example of the brain influencing sensory function is through circadian output to PRs (30).…”

Section: Discussionmentioning

confidence: 99%

Retrograde signaling from the brain to the retina modulates the termination of the light response in Drosophila

Rajaram

Scott

Nash

2005

Proc. Natl. Acad. Sci. U.S.A.

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A critical factor in visual function is the speed with which photoreceptors (PRs) return to the resting state when light intensity dims. Several elements subserve this process, many of which promote the termination of the phototransduction cascade. Although the known elements are intrinsic to PRs, we have found that prompt restoration to the resting state of the Drosophila electroretinogram can require effective communication between the retina and the underlying brain. The requirement is seen more dramatically with long than with short light pulses, distinguishing the phenomenon from gross disruption of the termination machinery. The speed of recovery is affected by mutations (in the Hdc and ort genes) that prevent PRs from transmitting visual information to the brain. It is also affected by manipulation (using either drugs like neostigmine or genetic tools to inactivate neurotransmitter release) of cholinergic signals that arise in the brain. Intracellular recordings support the hypothesis that PRs are the target of this communication. We infer that signaling from the retina to the optic lobe prompts a feedback signal to retinal PRs. Although the mechanism of this retrograde signaling remains to be discerned, the phenomenon establishes a previously unappreciated mode of control of the temporal responsiveness of a primary sensory neuron.acetylcholine ͉ electroretinogram ͉ general anesthetics ͉ photoreceptor

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Tachykinin-Related Peptide and GABA-Mediated Presynaptic Inhibition of Crayfish Photoreceptors

Cited by 53 publications

References 81 publications

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Identification and characterization of a tachykinin-containing neuroendocrine organ in the commissural ganglion of the crabCancer productus

Retrograde signaling from the brain to the retina modulates the termination of the light response in Drosophila

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