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Immediate Plasticity of Identifiable Synapses in the Land Snails Helix Lucorum

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Immediate Plasticity of Identifiable Synapses in the Land Snails Helix Lucorum Immediate plasticity of identifiable synapses in the land snails Helix lucorum Evgeni Sokolov and Tatiana Palikhova Department of Psychology, Moscow State University, 8 Mokhovaya St., 103009 Russia, Email: [email protected] Abstract. The data presented concern synaptic plasticity arising during neuronal response to a single sensory stimulus. The plasticity was studied in identifiable synapses between sensory and command neurones of Helix lucorum using simultaneous intracellular recording. A brief mechanosensory stimulation evoked a train of spikes in an identifiable visceral sensory neurone. Interspike intervals within the train changed from short (tens ms) to long (s). Each spike elicited an elementary EPSP in an identifiable command neurone. The amplitude of elementary EPSPs varied during a train of action potentials. Initial high frequency depression was followed by posttetanic potentiation and subsequent low frequency depression. The result of integration of the three pkastic processes has been named immediate plasticity. It has been shown that a compound EPSP elicited in a postsynaptic command neurone by a single sensory stimulus depends on the immediate plastic changes of elementary EPSPs. Key words: identifiable neurone. identifiable synapse, elementary EPSP, compound EPSP, immediate plasticity, synaptic depression, posttetanic potentiation 162 E. Sokolov and T. Palikhova INTRODUCTION Synaptic connections repeatedly identified in various preparations are termed identifiable synapses (Sokolov Plasticity of synapses presents a background for and Logunov 1985). The precondition to such regular learning and memory (Eccles 1964, 1993). Plasticity identification is based on identifiable neurones injected depends on sequence of stimuli. Sensory stimuli are by dyes (Arakelov and Sakharova 1982). Synapses be- usually used to test plastic modifications at both beha- tween sensory neurones representing internal organs and vioral and neuronal levels. The test stimuli for a single command neurones of defensive behaviour have been synapse are single presynaptic action potentials that anatomically identified in the land snail Helix (Arakelov evoke elementary postsynaptic potentials in follower et al. 199 1, Marakueva et al. 1992). Parallel injections of cells (Kandel 1976). A train of action potentials is a different dyes into a sensory neurone representing viscera typical response of neurones to a sensory stimulus. We of the animal (neuron LPa7) and the defensive command have suggested that each spike within a train evoked neurone (LPa3) have shown that the sensory neurone in a presynaptic neurone by a sensory stimulus pro- builds up 8-9 buttons on the dendrites of the command duces in a follower cell a change of synaptic efficacy. neurone (Marakueva et al. 1992). We have named these changes immediate plasticity The synapses between sensory cells and command (Palikhova and Sokolov 1997). We have also sug- neurones display several types of plastic changes (Logu- gested that a compound synaptic response of a postsy- nov 1984, Sokolov and Palikhova 199 1, Sokolov 1991 ). naptic cell to a single sensory stimuli depends on the This paper refers to a plasticity arising immediately after immediate plasticity of elementary postsynaptic single sensory stimulation of internal organs or direct potentials as well as on their space and time summa- electrical intracellular stimulation of an identified sen- tion. The goal of the present research was to test im- sory neurone. To test the immediate plasticity, double in- mediate plasticity at the synapses between identified tracellular recordings from sensory and command neurones in the land snail Helix lucorum. neurones in a semi-intact preparation were made during Molluscs, and snails in particular, are used as ex- sensory stimulation of the internal organs and during in- perimental model to study the mechanisms of plas- tracellular stimulation of a sensory neurone. It could be ticity at the behavioural, neuronal and synaptic levels shown that immediate plasticity revealed by a change of (Tauc 1966, Kerkut 1969, Sakharov and Shalanki elementary excitatory postsynaptic potential (eEPSP) is 1967, Sakharov 1974, 1994, Bullock and Basar 1988). the result of three types of processes: (1) initial short- Molluscs present a possibility to record electrical ac- -term depression of eEPSPs evoked by a high frequency tivity simultaneously from both pre- and postsynaptic train of action potentials, (2) following posttetanic neurones that can be activated by sensory stimulation potentiation of eEPSPs evident by a decrease of spiking (Kandel 1976, Byrn 1987, Sokolov 1991). Such a frequency and (3) subsequent low-frequency depression possibility is a necessary condition to study immediate or habituation of eEPSPs. plasticity. Synaptically connected identifiable neur- ones have been found in the central nervous system of METHODS the land snail Helix lucorum (Logunov and Balaban 1978)). It has been shown that some of the identified Preparation presynaptic cells are interceptive sensory neurones (Palikhova and Arakelov 1990, Sokolov 199 1). The Adult land snails Helix lucorum from a Crimea popu- postsynaptic cells are the command neurones that cen- lation were used. Experiments were performed on prep- tral the snail's escape behaviour (Sokolov 1977, Balaban arations consisting of central ganglia, mantle collar and 1979). It has been shown that elementary excitatory viscera (Palikhova and Arakelov 1990) and on modified postsynaptic potentials (eEPSPs) elicied at the com- "dissected foot" preparations (Shekhter 1980, Bravarenko mand neurones by the presynaptic spikes consist of et al. 1982, Arakelov et al. 199 1). The preparations were monosynaptic and polysynaptic components (Palikho- placed in a bath containing extracellular solution (in va et al. 1994). The monosynaptic components have mM): 80 NaC1,4 KCI, 8 CaC12,5 MgC12,4 Tris-HC1 (pH been proposed to be cholinergic (Ter-Markaryan et al. 7.8). Low-temperature (8-12OC) anaesthesia was used 1991) and consist of several subcomponents (Marakujeva during operations. Recordings were performed at room et al. 1992). (20-22OC) temperature. Immediate plasticity in Helix 163 Recording Stimulation Intracellular, somatic whole-cell current-clamp recor- Intracellular current injection and tactile stimulation dings were obtained simultaneously from the identified of the visceral organs were used to elicit spikes in the presynaptic and postsynaptic neurones. Identification of sensory neurones. Currents were injected into a cell the command and the sensory neurones was based on through the recording microelectrode by means of a morphological and physiological criteria (Arakelov et al. bridge circuit. Temporal parameters of the injected cur- 1991, Ierusalimski et al. 1994,Palikhova et al. 1994). In- rent depended on the experimental task. For rhythmic tracellular microelectrodes filled with 2.5 M KC1 had re- stimulation within a range of frequencies from 0.005 to sistance of 10-20 MR for pre- and 1-5 MR for 10 Hz short (5-50 ms) current pulses (1-10 nA) were postsynaptic neurones. The large soma size of command used. Direct current injections into the sensory neurone neurones, 200-300 ym, allowed us to use low-resistance had been used to trigger trains of presynaptic spikes that pipettes to record low-amplitude postsynaptic potentials. simulated trains of spikes elicited by sensory stimuli. Signals obtained from sensory and command neurones Calibrated hairs (0.1-0.2 mm 0.4-1.5 G) connected with were amplified with MEZ-8201 (Nihon Kohden, Japan) a solenoid and operated by an electrostimulator MSE-3R and MS-03 (Minsk, Belorus) amplifiers. Data were (Nihon Kohden, Japan) were used for sensory tactile stored on computer by an analog to digital converter and stimulation. program DS (Digiscope, Moscow) for monitoring, rec- Data from presynaptic sensory LPa7 and LPa9 and ording and subsequent analysis. postsynaptic command neurones LPa3 and RPa3 stu- FI~1 Monosynaptlcally connected ~dentifiable sensory (LPa7) and I 1 mV cornmand (LPa3) neurones are marked on a scheme of parietal iomplex gangha of Hel~xlucorum (A) that 1s a s~mpl~ficationof the / 20 mV lnap (Ierusal~msk~et a1 1992, 1994) based on the classical one (Sakharok - Is '~ndShalank~ 1969, Sakharok 1974) Detailed informat~onon the local~z- 'Ition of cell bod~esof the Identifled presynaptlc neurones can be found In (Arakelok et al 199 1, Palikho\ a et a1 1994) B. elementary EPSPs C ekoked In the command neurone by presynaptlc action potent~als ellcited by a mlcroplpette penetra- tlon into a presynaptlc neurone C, typ~calburst of spikes elicited by brief sensory stimulat~on(arrows) 10 mV In ~dentifiablesensory neurone and LPa7 typ~calcompound EPSP ekoked in 500 ms LPa3 command neurone by the sen- sory st~mulus 164 E. Sokolov and T. Palikhova died systematically were obtained in about 50 experi- to appreciate the contribution of single eEPSPs to ments. cEPSP. RESULTS Receptive field of an identifiable sensory neurone Elementary and compound postsynaptic Local tactile stimulation of different areas of the skin potentials and the internal organs demonstrated a "point-like" ex- citatory area of the sensory neurone surrounded by an in- Action potentials (APs) generated in an identifiable hibitory zone (Fig. 2A). The APs evoked by stimulation sensory neurone of a snail evoke elementary excitatory of the excitatory area were not preceded by EPSPs postsynaptic potentials (eEPSPs) in parietal command (Fig. 2B) indicating that they are
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