PHARMACOLOGICAL ANALYSIS OF THE CHOLINERGIC INPUT TO THE LOCUST VPLI NEURON FROM AN EXTRAOCULAR PHOTORECEPTOR SYSTEM

1. The brain of the locust contains an extraocular photoreceptor (EOP) , which provides the major synaptic excitation to the vasopressin-like immunoreactive (VPLI) interneuron of the suboesophageal ganglion. Alt hough the precise location of the EOP remains unknown, its activity ca n be determined indirectly by intracellular recording from the VPLI ne uron. The excitatory drive to the VPLI neuron occurs only in darkness and is absent in the light. 2. The EOP is preferentially sensitive to light of wavelength 494 +/ 7 (SD) nm (blue-green) and has an absorptio n spectrum characteristic of a rhodopsin-like photopigment. 3. In the presence of high divalent saline (20 mM Ca2+ and Mg2+), the VPLI neuro n receives excitatory input in the light. This indicates that the exci tatory input to the VPLI neuron is from a tonically active descending input, which normally is inhibited by the light-induced activation of the presynaptic EOP. 4. Stimulation of the connectives while recording the resultant excitatory postsynaptic potential (EPSP) evoked in VPLI shows that the descending input projects beyond the suboesophageal ga nglion, extending as far as the metathoracic ganglion. 5. Pharmacologi cal analysis shows that the descending input to the VPLI neuron is cho linergic: acetylcholine (ACh) strongly depolarizes the neuron and eser ine, an ACh esterase inhibitor, markedly potentiates the synaptic exci tation of the VPLI neuron. 6. Nicotinic and muscarinic receptor antago nists show that the excitation of VPLI consists of two pharmacological ly discrete components. Nicotinic ACh receptors mediate a fast depolar ization, whereas muscarinic ACh receptors evoke a more sustained depol arization. Accordingly, both a fast and slow depolarization can be evo ked selectively in VPLI by direct application of either nicotine or mu scarine. 7. Voltage-clamp analysis shows that the fast EPSP evoked cur rent is similar to that produced by nicotine in that it decreases line arly with membrane depolarization. The current associated with the sus tained depolarization is similar to that evoked by muscarine, increasi ng nonlinearly with membrane depolarization. 8. Activity of the descen ding input, or application of muscarine, lowers the spike-initiation t hreshold of the VPLI neuron, thereby increasing its excitability. 9. I t is concluded that the presence of two ACh receptor subtypes act syne rgistically to allow continuous activity of the VPLI neuron for sustai ned periods (i.e., throughout the hours of darkness).