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Nitric oxide induces centrally generated motor patterns in the locust suboesophageal ganglion

Georg F. Rast^*

Institut für Biologie II, Rheinisch-Westfälische Technische Hochschule Aachen, 52056 Aachen, Germany

View larger version (38K): [in a new window]   Fig. 1. Nitrergic and muscarinic pattern generation in the locust suboesophageal ganglion (SOG). (A) Diagrammatic dorsal view of the SOG showing nerves 1C (N1C) and 1D (N1D), from which mandibular opener and closer motor patterns were recorded. Nerves are numbered consecutively (see Altman and Kien, 1979). (B) Motor pattern induced by the NO donor hydroxylamine before (left) and after (right) application of the soluble guanylyl cyclase (sGC) inhibitor 1H-(1,2,4)oxa-diazolo(4,3a)-quinoxalin-1-one (ODQ). Upper trace, mandibular opener motor nerve; lower trace, mandibular closer motor nerve. (C) Motor pattern induced by the NO donor sodium nitroprusside (SNP) before (left) and after (right) application of the sGC inhibitor ODQ. (D) The motor pattern induced by SNP is not affected by the amount of dimethyl sulphoxide (DMSO) required to dissolve ODQ. (E) Motor pattern induced by the muscarinic agonist pilocarpine (left). After application of the muscarinic antagonist atropine, the pattern is abolished but reappears after washing and reapplication pilocarpine (right). (F) Motor pattern induced by the muscarinic agonist oxotremorine (left). After application of the muscarinic antagonist scopolamine, the pattern is abolished but reappears after washing and reapplication of oxotremorine (right). COC, circumoesophageal connectives; NC, neck connectives; N, nerve; cl mn, closer motor nerve; op mn, opener motor nerve.

View larger version (25K): [in a new window]   Fig. 2. Comparison of the characteristics of the nitrergic motor patterns determined from 50 s stretches of activity. Depending on the mean bursting frequency, this observation period covered 26–57 cycles. Asterisks mark significant differences (sign-test: P<0.05; N=5). (A) Frequency of bursting. (B) Mean duty cycle (burst duration divided by cycle period). (C) Intra-burst frequency. (D) Number of units distinguishable in the extracellular recordings by visual inspection. cl, closer; op, opener; Hydrox., hydroxylamine; ODQ, 1H-(1,2,4)oxa-diazolo(4,3a)-quinoxalin-1-one; SNP, sodium nitroprusside. Values are mean + S.D.

View larger version (31K): [in a new window]   Fig. 3. Comparison of characteristics of the muscarinic motor patterns determined from 50 s stretches of activity. Depending on the mean bursting frequency, this observation period covered 26–57 cycles. Asterisks mark significant differences (sign-test: P<0.05; N=5). (A) Frequency of bursting. (B) Mean duty cycle (burst duration divided by cycle period). (C) Intra-burst frequency. (D) Number of units distinguishable in the extracellular recordings by visual inspection. cl, closer; op, opener; atr., atropine; oxo., oxotremorine; pilo., pilocarpine; scop., scopolamine. Values are mean + S.D.

View larger version (28K): [in a new window]   Fig. 4. The motor patterns induced by muscarinic agonists and by nitric oxide are independent. (A) The generation of the motor pattern induced by the NO donor hydroxylamine (left) does not involve muscarinic signalling since it is not blocked by the muscarinic antagonist atropine. (B) The generation of the motor pattern induced by the NO donor sodium nitroprusside (SNP) does not involve muscarinic signalling, since it is not blocked by the muscarinic antagonist scopolamine. (C) The generation of the motor pattern induced by the muscarinic agonist pilocarpine does not involve NO signalling, since it is not blocked by the soluble guanylyl cyclase (sGC) inhibitor 1H-(1,2,4)oxa-diazolo(4,3a)-quinoxalin-1-one (ODQ). (D) The generation of the motor pattern induced by the muscarinic agonist oxotremorine does not involve NO signalling, since it is not blocked by the sGC inhibitor ODQ. cl mn, closer motor nerve; op mn, opener motor nerve; DMSO, dimethylsulphoxide.

View larger version (25K): [in a new window]   Fig. 5. Comparison of characteristics of the nitrergic motor patterns determined from 50 s stretches of activity in five preparations before and after application of muscarinic antagonists. Depending on the mean bursting frequency, the observation period covered 31–55 cycles. (A) Frequency of bursting. (B) Mean duty cycle (burst duration divided by cycle period). (C) Intra-burst frequency. (D) Number of units distinguishable in the extracellular recordings by visual inspection. cl, closer; op, opener; atr., atropine; hydrox., hydroxylamine; scop., scopolamine; SNP, sodium nitroprusside. Values are mean + S.D.

View larger version (30K): [in a new window]   Fig. 6. Comparison of characteristics of the muscarinic motor patterns determined from 50 s stretches of activity in five preparations before and after application of the soluble guanylyl cyclase inhibitor 1H-(1,2,4)oxa-diazolo(4,3a)-quinoxalin-1-one (ODQ). Depending on the mean bursting frequency, the observation period covered 31–55 cycles. (A) Frequency of bursting. (B) Mean duty cycle (burst duration divided by cycle period). (C) Intra-burst frequency. (D) Number of units distinguishable in the extracellular recordings by visual inspection. cl, closer; op, opener; oxo., oxotremorine; pilo., pilocarpine. Values are mean + S.D.

View larger version (70K): [in a new window]   Fig. 7. NADPH-diaphorase staining in horizontal sections of the suboesophageal ganglion (SOG). (A–C) Schematic drawings of the SOG in a ventral (A), dorsal (B) and lateral (C) view. For orientation, the cells shown in D–H are indicated by dots in the drawings (D in A, E–H in B). In C, the planes of sectioning for D–H are indicated. Anterior is to the top in all panels. (D) Ventral section with anterior groups of small cells (dashed circles). (E) Lateral anterior cells. (F) Lateral posterior cells. (G) Dorsal anterior medial cells. (H) Prominent neuropilar structures in a mid-ventral plane with the dense posterior -shaped neuropilar region showing fine processes and boutons and the anterior ventral mandibular neuropil (dashed line). N1–N7, nerves 1–7. Scale bars, 100 µm.

View larger version (73K): [in a new window]   Fig. 8. Cyclic-GMP-like immunoreactivity in the suboesophageal ganglion (SOG). (A–C) Schematic drawings of the SOG in a ventral (A), dorsal (B) and lateral (C) view. For orientation, the cells shown in D–H are indicated by dots in the drawings (D in A, E–H in B). In C, the planes of sectioning are indicated. Anterior is to the top in all panels. (D) Ventral section showing two very prominent cGMP-immunoreactive cells located between the roots of nerve 5. Note that this nerve also contains immunoreactive fibres. (E) Large anterior and lateral cGMP-immunoreactive neurones. (F) Dorsal anterior medial cells. (G) Ventral section showing immunoreactive fibres in the mandibular nerve (N1) and stained neuropilar regions along the midline. (H) Stained structures in the mandibular neuropil (anterior) and a posterior medial neuropilar area. N1–N7, nerves 1–7. Scale bars, 100 µm.

View larger version (83K): [in a new window]   Fig. 9. Identified suboesophageal ganglion (SOG) neurones showing anti-cGMP immunoreactivity. (A) Mandibular closer motoneurone injected with Lucifer Yellow and photographed with an appropriate filter set. (B) The same neurone shows anti-cGMP immunostaining (CY3-labelled secondary antibody photographed with an appropriate filter set). (C) Salivary neurone 1 (SN1) labelled by backfilling of nerve 7B with dextran-amine-conjugated Lucifer Yellow. (D) SN1 is anti-cGMP-immunoreactive. (E) Salivary neurone 2 (SN2) labelled by backfilling of nerve 7B with dextran-amine-conjugated Lucifer Yellow. (F) SN2 does not show anti-cGMP immunoreactivity. Scale bars, 100 µm.