The wind-sensitive cercal receptor/giant interneurone system of the locust,Locusta migratoria

Summary

• 1. The cercal receptor/giant interneurone system of the locustLocusta migratoria has been investigated with respect to input to giant interneurones (GINs) from wind-sensitive filiform hairs on the cercus. Each filiform hair is innervated by a single receptor neurone which is depolarized when the hair is deflected by wind or mechanical stimuli (Fig. 1A, B). The resulting action potentials travel in the cercal nerve with a velocity of 1.0±0.2 m/s and arrive in the terminal ganglion of the central nervous system 3.5±0.6 ms after stimulus onset (Figs. 1C, 2).

• 2. Within the terminal ganglion EPSPs are evoked 1∶1 in a giant interneurone (GIN) by action potentials in a filiform afferent (Fig. 3). Three of the 4 GINs in the terminal ganglion receive excitatory input from filiform afferents on both cerci — GIN 4 appears to receive little or no excitatory input from the ipsilateral cercus (Fig. 4). The input from several filiform afferents converges onto a given GIN (Fig. 5A), and dual recordings show that the same afferent can evoke EPSPs simultaneously in two GINs (Fig. 5B).

• 3. Each of the four GINs in the terminal ganglion has a characteristic response to wind directed at the cerci, however, they fall into two broad groups: GINs 1 and 3 are excited about equally by wind directed at either cercus, whereas GINs 2 and 4 are strongly excited by wind directed at the contralateral cercus but weakly, and with a mixture of excitation and inhibition, to wind directed at the ipsilateral cercus (Fig. 6). This is consistent with anatomical data. The responses of GIN 1 are phasic, those of the other GINs more tonic. Electrical stimulation of each cercal nerve evokes responses in the GINs which parallel those produced by wind. The EPSP evoked in each GIN by electrical stimulation of the cercal nerve does not decrement appreciably even at high (100 Hz) stimulus frequencies (Fig. 6).

• 4. Dual intracellular penetrations reveal synaptic connections between some of the GINs in the terminal ganglion (Fig. 7). In general: excitatory connections are only made between ipsilateral neurones; excitatory connections are unilateral, and from neurones with more posterior cell bodies to those with more anterior cell bodies; connections are strongest between neurones belonging to the same group with respect to the directionality of their responses to wind stimulation; reciprocal inhibitory connections occur between contralateral neurones of different type; and all connections result in only subthreshold postsynaptic activity. Dual penetrations of left and right partners of the same GIN type failed to reveal either spiking or graded interactions between them (Fig. 8).

• 5. Intracellular recordings from GINs in the terminal ganglion and simultaneous extracellular monitoring of action potentials in their axons in the ventral nerve cord gave conduction velocities of 2.6–4.0 m/s for the different GINs (Fig. 9). This correlates well with the measured axon diameter for each GIN.

• 6. In the case of GINs 1 and 4, dual intracellular recordings from the same cell (in the terminal ganglion and in the posterior part of the metathoracic ganglion) show that action potentials are conducted 1∶1 to the anterior electrode with a delay of approximately 6–8 ms (Fig. 10). Lucifer Yellow dye injected at both recording sites identified the cell and confirmed the metathoracic arborizations seen for each neurone in cobalt backfills (previous paper).