Neuronal sites of action of a neurosecretory peptide, egg-laying hormone, in Aplysia californica

Abstract

1. Egg-laying hormone (ELH) is a polypeptide of about 4,500 mol wt synthesized in the bag cell neurons of the abdominal ganglion of Aplysia. We studied the effects of ELH on the neuronal activity of the attached head ganglia (buccal, cerebral, pleural, and pedal), on the isolated buccal ganglia, as well as on feeding in intact Aplysia. 2. Starved animals (n = 7) injected with crude extract containing ELH stopped eating algae at 17 +/- 4 min and their eggs first appeared at 29 +/- 4 min after injection at 20 degrees C. This cessation of eating is significant when compared to the seven controls (P less than 0.01). These data clearly indicate that a suppression of feeding activity occurs before the appearance of eggs. 3. ELH applied to the paired buccal ganglia in vitro activates a pair of neurons into a tonic pacemaker mode (approximately 1 spike/s). This activation also occurs in a high-magnesium, zero calcium solution that blocks chemical synapses. The time for the full appearance of this activity in vitro correlates well with the time for suppression of feeding in vivo. Each of these neurons has an ipsilateral axon in buccal nerve 3. The neuron has been identified by intracellular recording. 4. ELH increases the rate of firing of a second pair of buccal neurons, each with an ipsilateral axon in the cerebrobuccal connective. 5. ELH, when applied to the attached head ganglia, causes large bursts of neuronal activity in pedal nerves to the foot and increased activity in the nerve to the penis; the relevant neurons remain to be identified. 6. These in vitro effects were produced by ELH partially purified from bag cell cluster homogenates using ammonium sulfate precipitation followed by anion exchange and gel filtration chromatography or by ELH released from activated bag cells in isolated abdominal ganglia and then purified by gel filtration. The isolated buccal ganglia effects have been confirmed with fully purified ELH. 7. The ELH effects on the in vitro nervous system support the hypothesis that ELH in vivo acts directly on the nervous system to suppress feeding activity, controlled by the buccal and cerebral ganglia. ELH may also produce characteristic movements of the head during egg laying, controlled probably by the pedal and cerebral ganglia.

Egg-laying hormone of Aplysia induces a voltage-dependent slow inward current carried by Na+ in an identified motoneuron.

“…Purified ELH induces egg-laying behavior when injected into a sexually mature Aplysia (10,11). In addition, an inhibition of feeding also occurs, which begins before the appearance of eggs in the genital groove and persists for the duration of egg-laying behavior (11).…”

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

“…4). Also, the ability of NO to substitute for attempts to swallow could not be attributed to induction of egglaying by NO (Miller et al 2008), and the inhibition of feeding by egg-laying (Stuart and Strumwasser 1980;Ram 1982Ram , 1983Teyke et al 1991), since other treatments causing egg-laying did not substitute for NO in causing memory (Fig. 1).…”

“…When lip stimulation is paired with injection of a NO donor, animals learn that food is inedible, indicating that NO substitutes for attempts to swallow (Katzoff et al 2006). However, memory arising from pairing a NO donor and stimulating the lips with food could be caused by NO initiating egg-laying, perhaps because egg-laying causes inhibition of feeding (Stuart and Strumwasser 1980;Ram 1982Ram , 1983Teyke et al 1991), and lip stimuli become associated with inhibition of feeding. If this were so, pairing lip stimulation with agents other than NO that cause egg-laying should also cause memory that food is inedible.…”

“…For example, treatment with a NO donor induces aspects of egg-laying (Miller et al 2008), a behavior that is incompatible with feeding (Stuart and Strumwasser 1980;Ram 1982Ram , 1983Teyke et al 1991). In addition, blocking NO release in quiescent animals induces food arousal (Miller et al 2009), indicating that background NO release inhibits feeding.…”

The kinematics of multifunctionality: comparisons of biting and swallowing inAplysia californica

“…At the same time, neural control that shuts down one set of behaviors when incompatible behaviors are to be performed by the same peripheral structures may also confer a selective advantage. Indeed, in Aplysia, egg-laying hormone not only induces egg laying movements of the feeding apparatus, but also suppresses the animal's own feeding responses (Stuart and Strumwasser, 1980), thus preventing an Aplysia from eating its own eggs and blocking its own reproduction. Similarly, Clione's slow swimming movements are completely inhibited by defensive withdrawal behaviors, during which its wings are strongly retracted (Norekian and Satterlie, 1996).…”