The effect of social experience on serotonergic modulation of the escape circuit of crayfish.

The neuromodulator serotonin has widespread effects in the nervous systems of many animals, often influencing aggression and dominance status. In crayfish, the effect of serotonin on the neural circuit for tailflip escape behavior was found to depend on the animal's social experience. Serotonin reversibly enhanced the response to sensory stimuli of the lateral giant (LG) tailflip command neuron in socially dominant crayfish, reversibly inhibited it in subordinate animals, and persistently enhanced it in socially isolated crayfish. Serotonin receptor agonists had opposing effects: A vertebrate serotonin type 1 receptor agonist inhibited the LG neurons in dominant and subordinate crayfish and had no effect in isolates, whereas a vertebrate serotonin type 2 receptor agonist enhanced the LG neurons' responses in all three types of crayfish. The LG neurons appear to have at least two populations of serotonin receptors that differ in efficacy in dominant, subordinate, and socially isolate crayfish.

The onset of response habituation during the growth of the lateral giant neuron of crayfish.

1. The postembryonic development of the crayfish LG tailflip command neuron's response to mechanosensory input was studied with standard electrophysiological techniques in animals between 1 and 12 cm long. 2. LG neurons are present in each abdominal hemisegment where they receive direct and indirect excitatory input from mechanosensory afferents. In both small and large crayfish, electrical stimulation of an abdominal ganglionic nerve containing those afferents evoked a compound excitatory postsynaptic potential (EPSP) with an early, reliable alpha component and a later, depression-prone beta wave. It is known that the alpha and beta components are produced by inputs from primary mechanosensory afferents and interneurons, respectively. 3. In crayfish < 2 cm long, LG was excited by the alpha component. When superthreshold, the alpha component triggered a single spike; additional excitation provided by the later beta wave presumably was preempted by refractoriness following the alpha spike and by recurrent inhibition of LG excited by the spike. LG was excited reliably by the alpha component in response to repeated superthreshold stimulation. 4. In crayfish between 2 and 3 cm, LG was excited more readily by the beta wave than by the alpha component. LG's beta spike response habituated to repeated stimulation at 1 Hz, and the beta EPSP depressed whereas the alpha component was largely unchanged. The appearance of the cellular substrates of habituation correlates with the reported onset of behavioral habituation of the tailflip response. Higher stimulus levels brought the alpha EPSP to threshold. Repetitive stimulation at these levels reliably evoked LG spikes from the alpha EPSP.(ABSTRACT TRUNCATED AT 250 WORDS)

Postsynaptic modulation of rectifying electrical synaptic inputs to the LG escape command neuron in crayfish.

The lateral giant (LG) tail-flip escape system of crayfish is organized to provide a massive convergence of mechanosensory inputs onto the LG command neuron through electrical synapses from both mechanosensory afferents and interneurons. We used electrophysiological techniques to show that the connections between three major mechanosensory interneurons and LG rectify, and that their inputs to LG can be reduced by postsynaptic depolarization and increased by postsynaptic hyperpolarization. The mechanosensory afferents and interneurons are excited by sensory nerve shock, and the components of the resulting LG PSP can be similarly modulated by the same postsynaptic potential changes. Because these inputs are all made through electrical synapses, we conclude that they are rectifying connections, as well. To test the physical plausibility of this conclusion, we developed an electrical model of the rectifying connection between a mechanosensory interneuron and LG, and found that it can reproduce all the qualitative features of the orthodromic and antidromic experimental responses. The ability of postsynaptic membrane potential to modulate inputs through rectifying electrical synapses is used in the escape system to enhance LG's relative sensitivity to novel, phasic stimuli. Postsynaptic depolarization of LG produced by earlier inputs "reverse-biases" the rectifying input synapses and reduces their strength relative to times when LG is at rest.

Development of habituation in the crayfish due to selective weakening of electrical synapses.

During posthatching development, transmission becomes substantially reduced at monosynaptic electrical synapses between tactile afferents and the command neuron for caudal tailflip escape responses of the crayfish. The effectiveness of a parallel disynaptic pathway to the same command neuron is unaltered during posthatching growth. In small crayfish both the monosynaptic and disynaptic sensory pathways can elicit command cell action potentials. At this stage, the characteristics of the tailflip neural circuit are evidently controlled by the shorter latency, non-labile monosynaptic pathway. Consequently, tailflips can be reliably elicited in young crayfish, even at brief (2 s) interstimulus intervals. Tailflip responses of large, older crayfish are known to habituate when tactile stimuli are repeated at intervals up to 5 min. This decline in behavioral responsiveness is presumed to be mediated by low frequency synaptic depression (LFD) at first-order synapses of the disynaptic pathway. The lability of these synapses does not change during post-hatching development. Weakening of the monosynaptic pathway may be caused by command cell growth during posthatching development.

Electrophysiology of dentate gyrus granule cells.

The orthodromic synaptic responses, membrane properties, and responses of dentate gyrus granule cells (DGCs) to several convulsant agents were studied in the in vitro hippocampal slice preparation. Orthodromic stimulation via the perforant pathway (PP) evoked excitatory-inhibitory postsynaptic potentials (EPSP-IPSP) sequences in 27 of 34 DGCs studied. In the majority, only one action potential could be evoked by supramaximal orthodromic stimulation. In recordings from DGC somata, overshooting spikes could be evoked either orthodromically or by current injections. Small-amplitude, fast transients were seen in 5 of 34 DGCs. The current/voltage (I-V) characteristic of most DGCs was linear throughout a range of membrane potentials between 15 and 20 mV negative and 5 and 15 mV positive to the resting potential. At the extremes of this range nonohmic behavior was noted. Exposure of slices to agents that block IPSPs, such as penicillin, bicuculline, picrotoxin, and media containing low Cl- concentrations, eliminated PP-evoked hyperpolarizations in DGCs and prolonged the repolarizing phase of the PP EPSP. In contrast to findings in hippocampal pyramidal cells and neocortical neurons, blockade of IPSPs did not lead to the development of orthodromically evoked slow depolarizations and burst discharges. After slices were exposed to 5 mM tetraethylammonium, current pulses evoked slow spikes, which were resistant to tetrodotoxin and presumably mediated by Ca2+. Spontaneous burst discharges or bursts evoked by brief depolarizing pulses did not occur under these conditions. Substitution of Ba2+ for Ca2+ in the perfusion solution resulted in development of spontaneous slow membrane depolarizations and burst discharges in DGCs. Burst discharges could be directly evoked and spikes were prolonged and resistant to tetrodotoxin (TTX). After hyperpolarizations lasting 200-1,000 ms, associated with a conductance increase and presumably due to a Ca2+-activated K+ conductance, followed directly evoked spike trains in 5 of 20 DGCs. These data suggest that Ca2+ conductances may be evoked in DGCs under certain circumstances but are not prominent during activation of DGCs under standard in vitro recording conditions.(ABSTRACT TRUNCATED AT 400 WORDS)

Release of 3H-gamma-aminobutyric acid (GABA) by inhibitory neurons of the crayfish.

Inhibitory neurons innervating the muscle receptor organ (MRO) of crayfish were used to study the uptake and release of tritiated GABA. MROs that have been directly exposed to 3H GABA for 60--75 min release radioactivity during low-frequency electrical stimulation. When ganglia containing the inhibitory cell bodies are exposed to 3H GABA, the isotope travels along a pathway unique to the inhibitory axon, at rates that range between 160 and 240 mm per day. Electrical stimulation of inhibitory axons whose cell bodies have been exposed to 3H GABA for 4--5 hr produces release of isotope from isolated MROs. Low calcium, high magnesium exposure prevents the stimulus-dependent release of radioactivity. Thin layer chromatographic analyses indicate that GABA comprises at least a major fraction of the radioactivity collected from stimulated preparations. A number of unidentified radioactive compounds are usually present with GABA, and it is suggested that most of these are catabolites of GABA.

Inhibition of mechanosensory interneurons in the crayfish. I. Presynaptic inhibition from giant fibers.

1. Sucrose-gap and intracellular recordings were used to study the primary afferent depolarization (PAD) produced in mechanosensory afferents by impulses in lateral and medial giant axons, which are the command cells for the tail flip escape response in the crayfish. 2. The lateral and medial giant axons produce PAD through a polysynaptic interneuronal pathway. The response has a relatively long intraganglionic latency (7--11 ms), and command-evoked PAD can be recorded in ganglia from which the giant axons have been experimentally disconnected. 3. The final neurons of the pathway that delivers inhibition are few in number and extensive in distribution; most appear to be common to lateral and medial giant pathways. 4. At least some of the inhibitory interneurons have axons in the interganglionic connectives and probably produce both presynaptic and postsynaptic inhibition. 5. Stimulation of the lateral, but not the medial, giant axons causes a small, short-latency deplorization that is stable at high repetition rates. This small potential can be accounted for by transmission across known electrical synapses between mechanosensory afferents and the lateral giants in each abdominal ganglion. 6. Repetitive stimulation of the lateral giant axons causes substantial augmentation of PAD, apparently through recruitment of additional interneurons. PAD evoked by a single medial giant (MG) stimulus is generally much larger than that elicited by a single lateral giant (LG) spike. However, MG-PAD summates little and so the maximum PAD deltaV reached during repetitive firing is equivalent for the two types of giant axons. 7. Iontophoresis of gamma-aminobutyric acid (GABA) into the ganglionic neuropil depolarizes the primary afferents and blocks activity in neurons that have axons in the interganglionic connective. 8. The extrapolated PAD reversal potential and pharmacological studies suggest that a GABA-mediated chloride conductance increase is involved in the production of PAD.