PLATEAU POTENTIALS IN AN INSECT MOTONEURONE CAN BE DRIVEN BY SYNAPTIC STIMULATION

1993 ◽  
Vol 176 (1) ◽  
pp. 307-310
Author(s):  
J. C. Hancox ◽  
R. M. Pitman

Cyclical patterns of behaviour such as respiration and locomotion are generated by groups of neurones whose output depends not only upon their synaptic interconnections but also on the intrinsic membrane properties of individual cells. For example, the ionic conductances of some neurones in rhythm-generating circuits allow these cells to respond to non-patterned excitatory synaptic drive with ‘plateau’ or ‘driver’ potentials: prolonged, regenerative depolarizations which can drive bursts of impulses and, thereby, contribute to characteristics of the motor rhythm (Russell and Hartline, 1978, 1982; Tazaki and Cooke, 1979a-c, 1983a-c, 1986, 1990). Plateau potentials are not restricted to interneurones of the central pattern generator; they may also be recorded from motoneurones, which form the final output to muscles. Thus, plateau potentials have been recorded from locomotor motoneurones from the crayfish (Sillar and Elson, 1986), lamprey (Wallen and Grillner, 1987), cat (Hounsgaard et al. 1988) and turtle (Hounsgaard and Kiehn, 1989) (see also review by Kiehn, 1991).

1994 ◽  
Vol 72 (6) ◽  
pp. 2827-2839 ◽  
Author(s):  
P. J. Istvan ◽  
P. Zarzecki

1. Discharge patterns of neurons are regulated by synaptic inputs and by intrinsic membrane properties such as their complement of ionic conductances. Discharge patterns evoked by synaptic inputs are often used to identify the source and modality of sensory input. However, the interpretation of these discharge patterns may be complicated if different neurons respond to the same synaptic input with a variety of discharge patterns due to differences in intrinsic membrane properties. The purposes of this study were 1) to investigate intrinsic discharge patterns of neurons in primary somatosensory cortex of raccoon in vivo and 2) to use somatosensory postsynaptic potentials evoked by stimulation of forepaw digits to determine thalamocortical connectivity for the same neurons. 2. Conventional intracellular recordings with sharp electrodes were made from 121 neurons in the cortical representation of glabrous skin of digit four (d4). Intracellular injection of identical current pulses (100-120 ms in duration) elicited various patterns of discharge in different neurons. Neurons were classified on the basis of these intrinsic patterns of discharge, rates of spike adaptation, and characteristics of spike waveforms. Three main groups were identified: regular spiking (RS) neurons, intrinsic bursting (IB) neurons, and fast spiking (FS) neurons. Subclasses were identified for the RS and IB groups. 3. Neurons were tested for somatosensory inputs by stimulating electrically d3, d4, and d5. Excitatory postsynaptic potentials (EPSPs) were elicited in 100% of the neurons by electrical stimulation of d4, the "on-focus" digit. EPSPs were usually followed by inhibitory postsynaptic potentials (IPSPs). Many neurons (41%) responded with EPSP-IPSP sequences after stimulation of d3 or d5, the "off-focus" digits. 4. Latencies of somatosensory EPSPs and IPSPs were used to determine the synaptic order in the cortical circuitry of RS, IB, and FS neurons. EPSPs with monosynaptic thalamocortical latencies were recorded in RS, IB, and FS neurons. 5. We conclude that precise patterns of neural discharge in primary somatosensory cortex cannot be reliable estimates of sensory inputs reaching these neurons because patterns of discharge are so strongly influenced by intrinsic membrane properties. Ionic conductances governing patterns of neuronal discharge seem almost identical in intact cortex of raccoon, rat, and cat, and in slices of rodent cortex, because similar patterns of discharge are found. The consistency of patterns of discharge across species and types of preparation suggests that these intrinsic membrane properties are a general property of cerebral cortical neurons and should be considered when evaluation sensory coding by these neurons.


1997 ◽  
Vol 200 (12) ◽  
pp. 1725-1736
Author(s):  
R Dicaprio

The motor neurons in the crab ventilatory system have previously been considered to be passive output elements in that the generation of bursts of action potentials in these neurons during ventilation was thought to be due to cyclic inhibition and excitation from the interneurons in the ventilatory central pattern generator. This study demonstrates that the large-amplitude depolarization that underlies bursts of action potentials in ventilatory motor neurons is produced by a plateau potential. These motor neurons satisfy a number of the experimental tests that have been proposed for plateau potentials, such as triggering of the burst by a brief depolarization, termination of the burst by a hyperpolarizing input, and an all-or-none suppression of the depolarizing potential by the injection of hyperpolarizing current.


2006 ◽  
Vol 96 (5) ◽  
pp. 2354-2363 ◽  
Author(s):  
Zhishang Zhou ◽  
Wenhui Xiong ◽  
Arjun V. Masurkar ◽  
Wei R. Chen ◽  
Gordon M. Shepherd

Understanding the intrinsic membrane properties of juxtaglomerular (JG) cells is a necessary step toward understanding the neural basis of olfactory signal processing within the glomeruli. We used patch-clamp recordings and two-photon Ca2+ imaging in rat olfactory bulb slices to analyze a long-lasting plateau potential generated in JG cells and characterize its functional input–output roles in the glomerular network. The plateau potentials were initially generated by dendritic calcium channels. Bath application of Ni2+ (250 μM to 1 mM) totally blocked the plateau potential. A local puff of Ni2+ on JG cell dendrites, but not on the soma, blocked the plateau potentials, indicating the critical contribution of dendritic Ca2+ channels. Imaging studies with two-photon microscopy showed that a dendritic Ca2+ increase was always correlated with a dendritic but not a somatic plateau potential. The dendritic Ca2+ conductance contributed to boosting the initial excitatory postsynaptic potentials (EPSPs) to produce the plateau potential that shunted and reduced the amplitudes of the following EPSPs. This enables the JG cells to act as low-pass filters to convert high-frequency inputs to low-frequency outputs. The low frequency (2.6 ± 0.8 Hz) of rhythmic plateau potentials appeared to be determined by the intrinsic membrane properties of the JG cell. These properties of the plateau potential may enable JG cells to serve as pacemaker neurons in the synchronization and oscillation of the glomerular network.


1993 ◽  
Vol 70 (3) ◽  
pp. 1030-1053 ◽  
Author(s):  
P. F. Rowat ◽  
A. I. Selverston

1. The gastric mill central pattern generator (CPG) controls the chewing movements of teeth in the gastric mill of the lobster. This CPG has been extensively studied, but the precise mechanism underlying pattern generation is not well understood. The goal of this research was to develop a simplified model that captures the principle, biologically significant features of this CPG. We introduce a simplified neuron model that embodies approximations of well-known membrane currents, and is able to reproduce several global characteristics of gastric mill neurons. A network built with these neurons, using graded synaptic transmission and having the synaptic connections of the biological circuit, is sufficient to explain much of the network's behavior. 2. The cell model is a generalization and extension of the Van der Pol relaxation oscillator equations. It is described by two differential equations, one for current conservation and one for slow current activation. The model has a fast current that may, by adjusting one parameter, have a region of negative resistance in its current-voltage (I-V) curve. It also has a slow current with a single gain parameter that can be regarded as the combination of slow inward and outward currents. 3. For suitable values of the fast current parameter and the slow current parameter, the isolated model neuron exhibits several different behaviors: plateau potentials, postinhibitory rebound, postburst hyperpolarization, and endogenous oscillations. When the slow current is separated into inward and outward fractions with separately adjustable gain parameters, the model neuron can fire tonically, be quiescent, or generate spontaneous voltage oscillations with varying amounts of depolarization or hyperpolarization. 4. The most common form of synaptic interaction in the gastric CPG is reciprocal inhibition. A pair of identical model cells, connected with reciprocal inhibition, oscillates in antiphase if either the isolated cells are endogenous oscillators, or they are quiescent without plateau potentials, or they have plateau potentials but the synaptic strengths are below a critical level. If the isolated cells have widely differing frequencies (or would have if the cells were made to oscillate by adjusting the fast currents), reciprocal inhibition entrains the cells to oscillate with the same frequency but with phases that are advanced or retarded relative to the phases seen when the cells have the same frequency. The frequency of the entrained pair of cells lies between the frequencies of the original cells. The relative phases can also be modified by using very unequal synaptic strengths.(ABSTRACT TRUNCATED AT 400 WORDS)


1983 ◽  
Vol 105 (1) ◽  
pp. 59-82
Author(s):  
P. S. Dickinson ◽  
F. Nagy

In the isolated stomatogastric nervous system of the lobster Fasus lalandii, the strong modifications of the pyloric motor pattern induced by firing of the single anterior pyloric modulator neurone (APM) are due primarily to modulation by APM activity of the regenerative membrane properties which are responsible for the ‘burstiness’ of all the pyloric neurones and particularly of the non-pacemaker neurones (constrictor motoneurones). This modulation has been studied under experimental conditions where the main extrinsic influences usually received by the pyloric constrictor neurones (intra-network synaptic interactions, activity of pacemaker neurones, and phasic central inputs from two premotor centres) are minimal. Under these conditions a brief discharge of neurone APM induces long plateaus of firing in all of the pyloric neurones. The non-pacemaker neurones of the pyloric network are not simply passive follower neurones, but can produce regenerative depolarizations (plateau potentials) during which the neurones fire spikes. The ability of the pyloric constrictor neurones to produce plateau potentials (plateau properties) contributes greatly to the generation of the rhythmical pyloric motor pattern. When these neurones spontaneously express their plateau properties, firing of neurone APM amplifies these properties. When most of the central inputs usually received by the pyloric constrictor neurones are experimentally suppressed, these neurones can no longer produce plateau potentials. In such conditions, firing of the single modulatory neurone APM can reinduce plateau properties of the pyloric constrictor neurones. In addition, firing in APM neurone slows down the active repolarization phase which terminates the plateau potentials of pyloric constrictor neurones. This effect is long-lasting and voltage-dependent. Modulation by APM of the plateau properties of the pyloric neurones also changes the sensitivity of these neurones to synaptic inputs. This effect can explain the strong modifications that an APM discharge exerts on a current pyloric motor pattern. Moreover, it might render the motoneurones of the pyloric pattern generator more sensitive to inputs from a command oscillator, and contribute to switching on the pyloric motor pattern.


1988 ◽  
Vol 136 (1) ◽  
pp. 53-87
Author(s):  
PATSY S. DICKINSON ◽  
FRÉDÉRIC NAGY ◽  
MAURICE MOULINS

In the red lobster (Palinurus vulgaris), an identified neurone, the anterior pyloric modulator neurone (APM), which has previously been shown to modulate the output of the pyloric central pattern generator, was shown to modulate the output of the gastric mill central pattern generator. APM activity induced a rhythm when the network was silent and increased rhythmic activity when the network was already active. Rhythmic activity was induced whether APM fired in single bursts, tonically or in repetitive bursts. A single burst in APM induced a rhythm which considerably outlasted the burst, whereas repetitive bursts effectively entrained the gastric oscillator. These modulations involved two major mechanisms. (1) APM induced or enhanced plateau properties in some of the gastric mill neurones. (2) APM activated the extrinsic inputs to the network, thus increasing the excitatory synaptic drive to most of the neurones of the network. As a result, when APM was active, all the neurones of the pattern generator actively participated in the rhythmic activity. By its actions on two separate but behaviourally related neural networks, the APM neurone may be able to control an entire concert of related types of behaviour.


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