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Inhibitory motor neurones supply body wall muscles in the locust abdomen

Michael Schmäh and Harald Wolf^*

Neurobiologie, Universität Ulm, D-89069 Ulm, Germany

View larger version (17K): [in a new window]   Fig. 1. Schematic diagram of the right set of body wall muscles in the locust abdominal segment 6, their inhibitory motor neuron supply, and the experimental arrangement. The body wall is shown flattened out, dorsal to the right and ventral to the left (nerve cord marks ventral midline), anterior to the top. Muscles are numbered according to Snodgrass (1935); 212, 213 and 214, dorsal, 217 and 218 ventral intersegmental muscles. Innervation by CIa is shown in red, by CIb, in green. Placement of intracellular recording electrodes is indicated in ventral and dorsal intersegmental muscles (FE1 and FE2, flexible electrodes) and in motor neuron soma (ME, microelectrode), allowing identification of inhibitory muscle innervation and staining of neurones by dye injection. An extracellular nerve recording (HE, hook electrode) monitored spike traffic through branches of nerve 1. The sixth abdominal segment is illustrated since it was in the focus of the present study, but the situation is identical in all other segments with unfused abdominal ganglia, and clear similarities exist in the remaining segments. For further details, see text. AG, abdominal ganglia; N, nerve.

View larger version (36K): [in a new window]   Fig. 7. Reconstruction in the frontal plane of a serially sectioned abdominal ganglion 5. Backfill of motor neurones through nerve 1 of abdominal ganglion 6 and subsequent GABA-immunocytochemistry identified the somata of CIa and CIb (black, straight arrow); the curved arrow indicates motor neuron somata without GABA immunoreactivity and the asterisk marks their primary neurites. The primary neurites of CIa and CIb leave their somata to loop dorsolaterally, crossing the ganglion midline in dorsal commissure V (DCV), and their axons project into the posterior connective via the dorsal intermediate tract (open arrow). Tracts and commissures are termed according to the nomenclature of Watson and Pflüger (1987). Dorsal is to the top. Scale bar, 50 µm.

View larger version (22K): [in a new window]   Fig. 2. Electrophysiological identification of muscle supply by inhibitory motor neurones. Top trace, intracellular soma recording from common inhibitor a (CIa); middle trace, extracellular recording from nerve 1 close to its exit from the sixth abdominal ganglion (N1AG6); bottom trace, intracellular recording from a muscle fibre in the dorsal intersegmental muscle 212a (M212a). Five sample recordings are superimposed, taking the largest spike in the nerve recording as reference. Note correspondence of, and constant time delay between, spikes in motor neuron and nerve recordings, and IPSP in muscle fibre recording.

View larger version (60K): [in a new window]   Fig. 3. Identification of inhibitory motor neurones CIa (i) and CIb (ii). (A) Intracellular recording from an inhibitory motor neuron's cell body (top traces) was combined with an extracellular recording from nerve 1 (or one of its branches; middle traces) and an intracellular recording from a target muscle (bottom traces) (experimental situation outlined in Fig. 1). 1:1 correspondence of spikes in motor neuron soma and nerve 1 with IPSPs in the muscle fibre recording indicated that the soma of an inhibitory motor neuron that supplies the muscle had been impaled (compare Fig. 2). (B) Dye was injected into the motor neuron soma to allow staining and morphological identification (see Materials and methods). (C) Current injection (bottom trace, e.g. in the context of staining CIa; other traces as in A) further verified the 1:1 correspondence of CI spikes and IPSPs noted above.

View larger version (41K): [in a new window]   Fig. 4. Activity pattern of inhibitory motor neurones in the ventilatory cycle. First (top) trace, extracellular recording from nerve 1 close to its exit from the sixth abdominal ganglion (N1AG6); middle trace, intracellular recording from a fibre in dorsal intersegmental muscle 212 (M212); bottom trace, intracellular recording from a fibre in ventral intersegmental muscle 217 (M217); below, expiration and inspiration phase of the ventilatory cycle obtained by optical monitoring. Activity of excitatory motor neurones is signified by prominent depolarisations during the expiration phase, activity of inhibitory motor neurones by smaller IPSPs, which are particularly evident due to summation at the beginning of the inspiration phase. Muscle 212 is supplied by CIa, muscle 217 by CIb (see Fig. 1).

View larger version (133K): [in a new window]   Fig. 5. Confocal microscopic images of abdominal ganglia 6 (A) and 7 (B) of the locust after backfilling of the right nerve 1 in abdominal ganglion 7 (red fluorescence, Ai,Bi,Ci) and GABA-immunocytochemistry (green fluorescence, Aii,Bii,Cii). Superposition of both labels is shown in Aiii,Biii,Ciii. There are only two somata in abdominal ganglion 6 that show the double label; they are located posteriorly, ventrally and contralaterally, and belong to CIa and CIb (arrowheads in Aiii). (C) Detail from a different preparation; abdominal ganglion 5, backfill in abdominal ganglion 6 (arrows indicate somata of CIa and CIb; ostensible double-labelling due to partial overlap of neighbouring red and green cells marked by open arrows). Two GABA-immunoreactive motor axons project to the periphery (arrows in A) through nerve 1 of each of the unfused abdominal ganglia. Asterisks in Aii and Aiii mark unspecific staining in nerve 2 of the sixth abdominal ganglion. Dotted lines indicate ganglion midlines. Scale bar, 100 µm (A,B); 20 µm (C).

View larger version (13K): [in a new window]   Fig. 8. Summary of inhibitory body wall motor neurones in the locust, incorporating data from other authors and possible homonomies. From the top, subesophageal (S1-3), thoracic (T1-3), fused (A1-3, A8-11) and unfused (A4-7) abdominal neuromeres and ganglia. Segmentally homologous (homonomous) inhibitory motor neurones are shown as outline sketches. Colour coding: red, CIa; green, CIb; yellow, `loop cell' of Kutsch and Heckmann (1995) (putative homologue of CIb); blue, `common contralateral A-type cell' of Steffens and Kutsch (1995) (putative homologue of CIa); orange, neuron after Bräunig (1993) and Bräunig et al. (2002); open circles, neurones predicted from present study. Scale bar, 200 µm.

View larger version (112K): [in a new window]   Fig. 6. Immunocytochemical identification of muscle supply by inhibitory motor neurones. Muscles of the abdominal body wall (muscle 218 is shown) were subjected to anti-GABA immunocytochemistry, which stained axons and terminals of the inhibitory motor neuron supply; branches of nerve 1B2 are shown here. Asterisks mark the disconnected ends of an originally continuous nerve branch. Scale bar, 50 µm.