Identified octopaminergic neurons provide an arousal mechanism in the locust brain

Abstract

1. Habituation is the declining responsiveness of a neural circuit (or behavior) to repetitive stimulation. Dishabituation (or arousal) can be brought about by the sudden presentation of an additional, novel stimulus. A clear example of arousal in the locust is provided by the visual system: the habituated response of the descending contralateral movement detector (DCMD) interneuron to repetitive visual stimuli can be dishabituated by a variety of other visual and tactile stimuli. 2. Application of octopamine to the locust brain and optic lobes dishabituates the DCMD in a manner similar to the effect of visual and tactile stimulation. 3. The locust CNS contains two pairs of octopamine-immunoreactive cells, the protocerebral medulla 4 (PM4) neurons, that could potentially mediate this dishabituation effect; PM4 neurons arborize in the optic lobe, they contain octopamine, and they respond to the same visual and tactile stimuli that dishabituate the DCMD. 4. To investigate whether PM4 activity dishabituates the DCMD, we recorded intracellularly from one of the PM4 neurons while recording extracellularly from the DCMD. When the PM4 neuron is injected with hyperpolarizing current to render it completely inactive, the DCMD exhibits its characteristic habituation to a moving visual stimulus. However, depolarizing the PM4 neuron, to produce action potentials at approximately 20 Hz, significantly increases the number of DCMD action potentials per stimulus. 5. The PM4 neurons may therefore play an important role in dishabituating the DCMD to novel stimuli. This effect is presumably mediated by PM4 neurons releasing endogenous octopamine within the optic lobe.