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Short-Term Dynamics of a Mixed Chemical and Electrical Synapse in a Rhythmic Network

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Short-Term Dynamics of a Mixed Chemical and Electrical Synapse in a Rhythmic Network The Journal of Neuroscience, October 22, 2003 • 23(29):9557–9564 • 9557 Behavioral/Systems/Cognitive Short-Term Dynamics of a Mixed Chemical and Electrical Synapse in a Rhythmic Network Akira Mamiya,1 Yair Manor,2 and Farzan Nadim3 1Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, New Jersey 07102, 2Life Sciences Department and Zlotowski Center for Neurosciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel 84105, and 3Department of Mathematical Sciences, New Jersey Institute of Technology, and the Department of Biological Sciences, Rutgers University, Newark, New Jersey 07102 In the rhythmically active pyloric circuit of the spiny lobster, the synapse between the lateral pyloric (LP) neuron and pyloric constrictor (PY) neuron has an inhibitory depressing chemical and an electrical component. To understand how the dynamics of the LP3PY synapse affect the relative firing times between these two neurons in an ongoing rhythm, we characterized the dynamics of the LP3PY synapse after a pharmacological block of ongoing activity. When a train of voltage pulses was applied to the voltage-clamped LP neuron, theinhibitorychemicalcomponentofthepostsynapticpotential(PSP)inthePYneuronrapidlydepressed.Thus,afterthefirstfewpulses, the PSP was either hyperpolarizing or depolarizing, depending on the interpulse duration, with shorter interpulse durations producing depolarizing PSPs. To characterize the synaptic response during rhythmic activity, we played back prerecorded realistic waveforms in the voltage-clamped LP neuron. After an initial transient, the resulting PSP in PY was always depolarizing, suggesting that in an ongoing rhythm, the electrical component of the synapse is dominant. However, our results indicate that the chemical component of the synapse acts to delay the peak time of the PSP and to reduce its amplitude, and that these effects become more important at slower cycle periods. Key words: synaptic depression; synaptic dynamics; stomatogastric ganglion; oscillations; central pattern generator; motor system Introduction pacemaker neurons with electrical and inhibitory chemical syn- Neurons coupled with electrical synapses often form chemical apses. The period and activity phase of pyloric neurons are deter- synapses as well (Michelson and Wong, 1994; Benardo, 1997; mined by the intrinsic properties of these neurons as well as the Gibson et al., 1999; Mann-Metzer and Yarom, 1999; Fukuda and dynamics of the synapses among them (Nusbaum and Beenhak- Kosaka, 2000). The composite “mixed synapse” is considered a ker, 2002). single functional unit. Several studies have proposed that mixed An important property of the pyloric network is that the rel- synapses act to synchronize the firing of neurons (Benardo, 1997; ative phase of activity of different neurons in the network is ad- Galarreta and Hestrin, 1999; Tamas et al., 2000) or serve as a justed depending on the cycle frequency to maintain a stable coincidence-detection mechanism of excitatory inputs (Galar- triphasic pattern (Miller and Selverston, 1982). Two classes of reta and Hestrin, 2001a). Mixed synapses have also been impli- follower neurons, the lateral pyloric (LP) and pyloric constrictor cated in neuronal rhythmogenesis (Galarreta and Hestrin, (PY) neurons, are reciprocally coupled via mixed synapses. In the 2001b). In many mixed synapses, the chemical component shows transmission of signals from the LP neuron to the PY neuron, the short-term facilitation or depression, whereas the effect of elec- two components of the mixed synapse have opposite effects. trical synapses is less use dependent (Galarreta and Hestrin, 1999; When the LP neuron bursts, the electrical component promotes Gibson et al., 1999; Tamas et al., 2000). Thus, a mixed synapse PY neuron activity, whereas the chemical component acts to sup- might dynamically change its properties in response to a modifi- press it. Moreover, previous studies have shown that the relative cation in the frequency or pattern of activation of the synapse phase of activity of the LP and PY neurons was well maintained (Galarreta and Hestrin, 2001b). when the frequency of the pyloric rhythm was altered by external We explore this possibility using the rhythmically active pylo- manipulation (Hooper, 1997a,b). ric network (frequency, 0.5–2 Hz) of the spiny lobster Panulirus In this study, we explore the complex interaction between interruptus. The pyloric rhythm is generated by a pacemaker en- electrical and inhibitory chemical components in the LP3PY semble of an anterior burster (AB) and two pyloric dilator (PD) synapse. We first characterize parameters describing the dynam- neurons. The remaining (follower) neurons are coupled to the ics of the synapse (amplitude and the extent and time constant of depression) by suppressing the pyloric activity, voltage clamping the LP neuron with trains of voltage pulses, and recording the Received June 24, 2003; revised Aug. 15, 2003; accepted Aug. 28, 2003. postsynaptic potential (PSP) in the PY neuron. After determining This research was supported by United States–Israel Binational Science Foundation Grant 2001-039 (Y.M. and the synaptic parameters, we describe the synaptic activity in the F.N.) and National Institute of Mental Health Grant 60605-01 (F.N.). context of the rhythmic pyloric rhythm. This is done by playing Correspondence should be addressed to Farzan Nadim, Department of Biological Sciences, 101 Warren Street, Newark, NJ 07102. E-mail: [email protected]. back prerecorded realistic waveforms in the voltage-clamped LP Copyright © 2003 Society for Neuroscience 0270-6474/03/239557-08$15.00/0 neuron and recording the PSP. Finally, using correlation analysis, 9558 • J. Neurosci., October 22, 2003 • 23(29):9557–9564 Mamiya et al. • Dynamics of a Mixed Synapse in a Rhythmic Network we show that the frequency-dependent properties of the LP3PY mixed synapse are important in determining the firing phase of the PY neurons during rhythmic activity. These results indicate that dy- namic properties of a mixed synapse can serve as a mechanism for fine-tuning of phasing in oscillatory networks. Materials and Methods All experiments were done on adult spiny lob- sters P. interruptus (Don Tomlinson Fisheries, San Diego, CA).The stomatogastric nervous system (STNS) was isolated with standard pro- cedures (Selverston et al., 1976; Harris-Warrick et al., 1992). The isolated STNS was pinned down on a Sylgard-coated Petri dish and super- fused with chilled (16°C) physiological saline containing the following (in mM): 479 NaCl, ⅐ ⅐ 12.9 KCl, 13.7 CaCl2 2H2O, 10 MgSO4 7H2O, 3.9 NaSO ⅐10 H O, 11.2 Trizma base, and 5.1 4 2 Figure1. Thepyloricnetworkgeneratesatriphasicrhythm.A,Intracellularvoltagetracesfromthepyloricnetworkpacemaker maleic acid, pH 7.45. neuron AB, the LP, and two PY neurons (PY1 and PY2). Bursting activity in the AB neuron is followed by (with a delay) a burst of Pyloric neurons were identified by their action potentials in the LP neuron and by (with some overlap) bursts of action potentials in the PY neurons. B, Circuit diagram stereotypical axonal projections in identified shows the connectivity among the AB, PD, LP, and PY neurons. Stimulating and recording electrodes were used in the LP neuron. nerves using conventional techniques (Selver- Recording electrodes were used to monitor the PY responses. C, Diagram indicating how the phase of the PY neuron burst onset ston et al., 1976; Harris-Warrick et al., 1992). was calculated with respect to the LP neuron burst onset during an ongoing pyloric activity. The phase is equal to the time The pyloric activity was monitored with difference between the two burst onsets divided by the pyloric cycle period. stainless-steel wire electrodes from identified nerves. Extracellular signals were amplified with a differential AC amplifier (model 1700; A-M systems, Carlsborg, experiments. A comparison with LP neuron waveforms recorded from WA). Intracellular recordings were made by impaling the soma with several experiments shows that these waveforms are representative of the LP neuron activity (data not shown). Note that the fact that we filter the sharp microelectrodes filled with 0.6 M K2SO4 plus 20 mM KCl (25–35 M⍀ for identification of neurons and for recording the postsynaptic waveforms and the filtering caused by the electrotonic structure of the LP neuron cause the chemical component of the synapse to be underesti- neuron) or 3 M KCl (8–12 M⍀ for current injection in the presynaptic neuron). All intracellular recordings were done with Axoclamp 2B am- mated. This point is addressed in the Discussion. Manipulations of traces plifiers (Axon Instruments, Foster City, CA). (waveform cutting, low-pass filtering, and averaging) were done with a Synaptic potentials were measured after abolishing the pyloric activity. custom-made program written in LabWindows/CVI (National Instru- ments, Houston, TX). This was done by bath application of 0.1 ␮M tetrodotoxin (TTX) (Bi- otium, Hayward, CA) to block both descending inputs to and activity All intracellular recordings were digitized at 4 kHz and stored on a within the stomatogastric ganglion. As expected, TTX eliminated the personal computer using a PCI-MIO-16E-1 board (National Instru- spike-mediated component of the LP3PY synapse. For technical rea- ments) and custom-made recording software written in LabWindows/ sons, we measured synaptic transmission in TTX so that presynaptic CVI (National Instruments). All analyses, such as detection of the peak release could
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