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Link to original content: https://pubmed.ncbi.nlm.nih.gov/8756451
Haltere afferents provide direct, electrotonic input to a steering motor neuron in the blowfly, Calliphora - PubMed Skip to main page content
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. 1996 Aug 15;16(16):5225-32.
doi: 10.1523/JNEUROSCI.16-16-05225.1996.

Haltere afferents provide direct, electrotonic input to a steering motor neuron in the blowfly, Calliphora

A Fayyazuddin  1 , M H Dickinson
Affiliations

Haltere afferents provide direct, electrotonic input to a steering motor neuron in the blowfly, Calliphora

A Fayyazuddin et al. J Neurosci. .

Abstract

The first basalar muscle (b1) is one of 17 small muscles in flies that control changes in wing stroke kinematics during steering maneuvers. The b1 is unique, however, in that it fires a single phase-locked spike during each wingbeat cycle. The phaselocked firing of the b1's motor neuron (mnb1) is thought to result from wingbeat-synchronous mechanosensory input, such as that originating from the campaniform sensilla at the base of the halteres. Halteres are sophisticated equilibrium organs of flies that function to detect angular rotations of the body during flight. We have developed a new preparation to determine whether the campaniform sensilla at the base of the halteres are responsible for the phasic activity of b1. Using intracellular recording and mechanical stimulation, we have found one identified haltere campaniform field (dF2) that provides strong synaptic input to the mnb1. This haltere to mnb1 connection consists of a fast and a slow component. The fast component is monosynaptic, mediated by an electrical synapse, and thus can follow haltere stimulation at high frequencies. The slow component is possibly polysynaptic, mediated by a chemical synapse, and fatigues at high stimulus frequencies. Thus, the fast monosynaptic electrical pathway between haltere afferents and mnb1 may be responsible in part for the phase-locked firing of b1 during flight.

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Figures

Fig. 1.
Fig. 1.
A, Experimental configuration for intracellular recording of mnb1. The preparation was perfused to allow constant exchange of solution. Suction electrodes were placed on the b1 nerve to record the activity of the mnb1 axon, and on the haltere nerve (HN) to record the response of haltere afferents.B, Diagram of Calliphora thoracic ganglion showing location of the mnb1. The arrowhead marks the putative recording site on the dendrite. The morphology of mnb1 is based on DAB-reacted biotinylated dextran back-fills of the b1 nerve and intracellular injections of neurobiotin. The identity of mnb1 in intracellular recordings was verified physiologically as explained in Materials and Methods. ADMN, Anterior dorsal mesothoracic nerve; PDMN, posterior dorsal mesothoracic nerve.
Fig. 2.
Fig. 2.
Response of mnb1 to mechanical oscillation of the haltere. Bottom trace shows the voltage used to drive the piezoelectric crystal attached to the haltere stalk. The middle trace shows phase-locked compound action potentials in the haltere nerve in response to haltere oscillation. The top trace is an intracellular recording from mnb1. Oscillation of the haltere produces a single subthreshold compound EPSP in every stimulus cycle. Occasionally, the EPSP crosses threshold and the mnb1 fires an action potential.
Fig. 3.
Fig. 3.
Mapping of haltere fields onto mnb1. A, Stimulation of single campaniform sensilla in dF2 produces a unitary EPSP in mnb1. The bottom trace shows a single extracellularly recorded action potential in the haltere nerve that is followed by a small EPSP in mnb1 (top trace). This figure is an average of 13 sweeps. B, Ablation of dF2 eliminates haltere-synchronous EPSPs in mnb1. The top pair of traces are controls that were recorded before ablation of dF2 and show haltere-synchronous EPSPs in mnb1 and a full complement of compound action potentials in the haltere nerve. After ablation of dF2 (bottom pair of traces), mnb1 shows no haltere-synchronous activity. In addition, the ablation of dF2 changes the sizes of compound action potentials within the haltere nerve recording.C, In this experiment, all fields have been ablated except for dF2. The haltere nerve now contains only one major compound action potential that occurs just before each EPSP in mnb1. The time and voltage scales in C are the same as those inB.
Fig. 4.
Fig. 4.
Frequency dependence of haltere-synchronous EPSPs in mnb1. Electrical stimulation of the haltere nerve produced a biphasic EPSP in mnb1 consisting of a fast superthreshold event followed by a smaller, slow event. Low-frequency stimulation at 1 Hz (shown in the left panel) produces no change in the EPSP from stimulus to stimulus. The middle panel shows the response of mnb1 to 10 Hz electrical stimulation of the haltere nerve, and the right panel shows the response to 100 Hz stimulation. After the first stimulus, the slow EPSP is still present during 10 Hz stimulation, whereas at 100 Hz it is greatly attenuated. All panels in this figure consist of five consecutive overlaid sweeps.
Fig. 5.
Fig. 5.
Effect of elevating threshold on the compound EPSP. A, Perfusion with saline containing three times the normal concentration of divalents. As the saline washes in, the spike in mnb1 completely disappears leaving just the EPSP. B, High-frequency stimulation (100 Hz) of the haltere nerve has no effect on the fast component of the EPSP (superposition of 10 consecutive stimulus cycles).
Fig. 6.
Fig. 6.
Effect of removing Ca2+ from the bath. In this experiment, the membrane response is entirely subthreshold, so no action potentials are masking the slow component. In the presence of Ca2+-free saline, the slow component completely disappears, whereas the fast component is unaffected. The slow component reappears when the Ca2+-free saline is replaced with normal saline.
Fig. 7.
Fig. 7.
Hypothesis that might explain how convergent mechanosensory input determines the firing phase of mnb1 during flight. The drawings are a schematic representation of the hypothesis, not actual data or the result of computer simulations. Both wing and haltere afferents provide an excitatory synaptic drive to mnb1, but the input from the two modalities arrives at different times within the stroke cycle. During stable flight, the firing phase of mnb1 is determined by the strong input from the wing afferents. During flight perturbations, recruitment of dF2 campaniforms causes the haltere input to be transiently stronger, thereby advancing the phase of mnb1. As the perturbation is corrected, the phase of mnb1 firing is once again determined by wing input. HN, Haltere nerve; WN, wing nerve.
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