Integrative Neurophysiology of the Lobster Cardiac Ganglion
TL;DR: The overall view is of a two-layered neural system in which the small cells possess an endogenous oscillatory driver potential, synchronized by synaptic and electrotonic interac?
Abstract: synopsis. The synchronized bursts of impulses produced by the nine neurons of the isolated Homarus cardiac ganglion are usually initiated by Cell 7. Activity in all other cells commences with very short latency thereafter. Impulses in most cells originate in trigger zones located 1-2 mm from the cell body, but the first several impulses in Cells 8 and 9 frequently originate in distal trigger zones some distance from the somata. Large cells fire at a high initial frequency, dropping rapidly to a low frequency plateau. Small cells exhibit a more tonic behavior and fire at intermediate rates. More anterior small cells tend to fire faster than more posterior ones. The major synaptic interactions are the impulse-mediated excitatory ones from small cells to large cells, and possibly to more anterior small cells. There are weak interactions from large cells back onto small cells, and very specific interactions from Cells 1 and 2 onto 3A, 4A, 5A, and 3B, 4B, 5B respectively. The large discrete EPSPs generated in large cells by small cell impulses appear to be the explanation for "discrete positioning" in large-cell firing patterns. In this situation, large-cell impulses only fire at discrete times during the burst, regardless of the actual large-cell pattern. The overall view is of a two-layered neural system in which the small cells possess an endogenous oscillatory driver potential, synchronized by synaptic and electrotonic interac? tions, and driving a train of impulses in each cell. This activates excitatory synapses on the large cells, which combined with a triggered driver potential in each large cell, produces synchronized trains of motor impulses which activate the heart muscle, causing the heart? beat.
Citations
More filters
TL;DR: Evidence of this permits resolution of the long-standing controversy over the neural basis of rhythmic behavior and aids in the identification of this mechanism as a general principle of neural organization applicable to all animals with central nervous systems.
Abstract: Timing of the repetitive movements that constitute any rhythmic behavior is regulated by intrinsic properties of the central nervous system rather than by sensory feedback from moving parts of the body. Evidence of this permits resolution of the long-standing controversy over the neural basis of rhythmic behavior and aids in the identification of this mechanism as a general principle of neural organization applicable to all animals with central nervous systems.
1,097 citations
TL;DR: The results show that the motor pattern produced by this well-studied central pattern generator circuit is highly plastic and can be modulated by endogenous biogenic amines.
Abstract: We investigated the effects of dopamine, octopamine, and serotonin on the motor output of the pyloric circuit in the stomatogastric ganglion of the lobster, Panulirus interruptus. Amines were bath applied at concentrations from 10(-8) to 10(-4) M, and the responses of the six classes of pyloric neurons were monitored both intracellularly and extracellularly. Each amine modified the pyloric motor pattern in a specific way. In addition, dopamine and octopamine were each able to produce different motor patterns at different concentrations. Amine effects on pyloric neurons included initiation and enhancement or inhibition of spike activity, changes in the phase relationships of neurons, and changes in the cycle frequency of the pyloric rhythm. These results show that the motor pattern produced by this well-studied central pattern generator circuit is highly plastic and can be modulated by endogenous biogenic amines.
216 citations
TL;DR: The role played by serotonin in the generation and modulation of behaviour in successively more complex species, ranging from coelenterates to humans is examined.
Abstract: Serotonergic neurons are present in all phyla that possess nervous systems. In most of these phyla, serotonin modulates important behaviours, including feeding, sexual and aggressive behaviour. Serotonin exerts its effects by acting in three basic modes: as a classical neurotransmitter, as a neuromodulator, or as a neurohormone. In a number of invertebrate species, the neural circuitry underlying the effects of serotonin has been well characterized, whereas in vertebrates, the mechanisms by which serotonin affects behaviour are currently less fully understood. The following review examines the role played by serotonin in the generation and modulation of behaviour in successively more complex species, ranging from coelenterates to humans.
161 citations
TL;DR: Certain properties of the system enhance switch-like on/off activity in each cell, which could contribute to burst generation and to appropriate phasing of bursts in the activity cycle.
Abstract: 1. Results from the companion paper were incorporated into a physiologically realistic computer model of the three principal cell types (PD/AB, LP, PY) of the pyloric network in the stomatogastric ganglion. Parameters for the model were mostly calculated (sometimes estimated) from experimental data rather than fitting the model to observed output patterns. 2. The initial run was successful in predicting several features of the pyloric pattern: the observed gap between PD and LP bursts, the appropriate sequence of the activity periods (PD, LP, PY), and a substantial PY burst not properly simulated by an earlier model. 3. The major discrepancy between model and observed patterns was the too-early occurrence of the PY burst, which resulted in a much shortened LP burst. Motivated by this discrepancy, additional investigations were made of PY properties. A hyperpolarization-enabled depolorization-activated hyperpolarizing conductance change was discovered which may make an important contribution to the late phase of PY activity in the normal burst cycle. Addition of this effect to the model brought its predictions more in line with observed patterns. 4. Other discrepancies between model and observation were instructive and are discussed. The findings force a substantial revision in previously held ideas on pattern production in the pyloric system. More weight must be given to functional properties of individual neurons and less to properties arising purely from network interactions. This shift in emphasis may be necessary in more complicated systems as well. 5. An example has been provided of the value quantitative modeling can be to network physiology. Only through rigorous quantitative testing can qualitative theories of how the nervous system operates be substantiated.
132 citations
References
More filters
TL;DR: Findings emphasize the role of cellular properties as compared to synaptic wiring in the production of cyclic motor patterns by ensembles of neurons in the lobster stomatogastric ganglion.
Abstract: Many of the motor neurons in the lobster (Panulirus interruptus) stomatogastric ganglion exhibit plateau potentials; that is, prolonged regenerative depolarizations resulting from active membrane properties, that drive the neurons to fire impulses during bursts. Plateaus are latent in isolated ganglia but are unmasked by central input. These findings emphasize the role of cellular properties as compared to synaptic wiring in the production of cyclic motor patterns by ensembles of neurons.
255 citations
TL;DR: In the heart of the Decapod Crustacea three systems of nervous elements can be distinguished, viz. a local system of neurons which are distributed in the heart itself, a system of fibres connecting the heart with the central nervous system, and a network of nerves which supply the valves of the arteries arising from the heart as well as the muscles of the pericardium.
Abstract: The results of our investigations may be summarized as follows: (1) In the heart of the Decapod Crustacea three systems of nervous elements can be distinguished, viz. ( a ) a local system of neurons which are distributed in the heart itself; ( b ) a system of fibres connecting the heart with the central nervous system; and ( c ) a system of nerves which supply the valves of the arteries arising from the heart as well as the muscles of the pericardium. (2) The local nervous system consists of a nervous trunk situated in the dorsal wall of the heart near to its inner surface from which branches to the muscle-fibres of the heart are distributed. The main trunk is generally called the ganglionic trunk from the presence of nerve-cells in it. The cells are of two kinds: large and small. Their number was found to be constant, and comprises in Cancer pagurus, Maia squinado, and Homarus vulgaris--the species which could be best investigated as to this point--nine elements., viz. five large and four small cells. It seems that in other species of marine Decapods the number of cells in the hearts, if not the same, does not at any rate vary much. Potamobius, however, has not less than sixteen elements (eight large, and eight, maybe, nine or ten, small ones). The cells are multipolar in shape. Their long processes--the axons--after sending out shorter ramifications run in regular courses, giving off long branches to all the muscles of the heart including those of the ostia, but excluding the muscle-fibres of the arterial valves. The short processes, which I regard as dendrites, spring from the cell-bodies and from the proximal parts of the axons. The endings of the dendrites which ramify in the muscle-bundles differ in appearance from the terminations of the long branches springing from the axons. The small cells possess similar processes, i.e. dendrites and axons. The latter could not be traced well. In the main or ganglionic trunk which in different species has different shapes, the following elements are present: ( a ) large and small cells, the arrangement of which varies in different species, but in all cases the small cells are situated in the posterior part of the trunk; ( b ) the axons of the large and small cells and a part of their branches; ( c ) the fibres of the dorsal nerves; ( d ) the neuropile-like networks of fibrils where the synapses between the efferent fibres and the neurons of the local system take place. These neuropiles form several more compact masses in Brachyura whilst in Macrura they are more diffusely scattered in the ganglionic trunk. (3) The fibres connecting the heart with the central nervous system take their origin in the infra-oesophageal ganglion and travel in the nerves running on the thoracic muscles. As separate bundles, one on each side, they turn towards the dorsal surface of the heart; hence the term nervi cardiaci dorsales is proposed; the other term--regulator nerves--indicates their physiological character. In their further course these nerves pierce the heart-wall and reach the local nervous system. The fibres of the dorsal nerves are of various diameters. The thicker, which in the description have been called System I, run throughout the ganglionic trunk and break up therein in many richly arborizing branches which at many places resemble in appearance the neuropile-like networks of fibrils. They are the fields of conjunction of all the fibres of System I with each other, as well as with the neurons of the local system. From the latter the following parts are in close relation with the fibrils of System I: ( a ) the collaterals of the axons entering the neuropile; ( b ) the dendrites; ( c ) the cell-bodies surrounded by a network of fibrils of the dorsal nerves; these basketworks, however, could not be seen in all the species investigated, and occur on the large cells only. Some branches of System I were found leaving the ganglionic trunk, but their destination is uncertain. The remaining fibres of the dorsal nerves which, it may be assumed, do not belong to the System I are of smaller but not equal diameter. Some take their course to the muscles without entering the ganglionic trunk, others travel in the latter, but their distribution could not be made out. (4) The third system of nerves, which enter into relationship with the heart by innervating the valves situated at the origin of the main arterial trunks, contains the following elements: ( a ) Nervi segmentales cord is, which number, as was found in Astacus, four on each side, branch from the thoracic nerves and pass on the ventral side of the pericardium towards the middle line. Here they join into--according to the species--one or two bundles, which take a longitudinal course. From these bundles branches are given off to the valves of five arteries, viz. arteriae antennales, arteriae hepaticae, and aorta posterior, and to the muscles of the ventral pericardial plate. The latter receive also branches springing directly from the segmental nerves. The system of the segmental nerves of the heart is connected with the nerves of the dorsal abdominal artery which in its turn receives segmental nerves originating in the abdominal ganglia and ending in the valves of the arteries arising from the vessel named. ( b ) The nervus cardiacus anterior arises from the stomatogastric nerve and runs alongside the median anterior artery. The territory of the terminal branches of this nerve, known as ‘nerf cardiaque’ of Lemoine, has been found to be confined entirely to the valve of the median anterior vessel (aorta anterior s. arteria ophthalmica). No connexion with the nerves of other valves could be ascertained. (5) Besides the three nervous systems enumerated which are in relation with the heart itself, several nerve branches running from the thoracic nerves penetrate the pericardial cavity. They break up here in the neuropile-like networks situated on the so-called ligaments of the heart and on the connective tissue covering the dorsal wall of the heart. (6) The probable function of all these elements is thought to be as follows: The local system is an ‘autonomic’ nervous apparatus from which the muscles of the heart receive impulses necessary for their regular contractions. The fact that the dendrites of the cells end in the muscles suggests that the rhythmical discharges in the nerve-cells are under the influence of the rhythmical action of the muscles. Thus, there may be secured a reciprocal regulation of the process in two parts of the neuromuscular apparatus of the heart. The dorsal nerves convey to the heart the inhibitory and accelerator fibres. Some evidence seems to indicate that the thicker fibres which have been found giving synapses with the neurons of the local system are endowed with the inhibitory function. The nerves of the arterial valves may be considered as carrying impulses which hold the muscle-fibres in contraction during the diastolic period of the heart. The nerves in the pericardial cavity, ending in fine networks, have evidently some sensory function.
156 citations
TL;DR: Voltage clamping giving step commands reveals a steady-state negative resistance characteristic in the current-voltage curves of Aplysia bursting neurons, observed below spike threshold in the unstable range through which the membrane potential slowly oscillates.
Abstract: Voltage clamping giving step commands reveals a steady-state negative resistance characteristic in the current-voltage curves of Aplysia bursting neurons This is observed below spike threshold in the unstable range through which the membrane potential slowly oscillates The negative resistance characteristic underlies this instability and shapes the rapid depolarization-hyper-polarization phase of the cycle When bursting cells are converted to silent cells (by cooling) the negative resistance is abolished; conversely, when normally silent cells are made to burst (by warming) a negative resistance develops The presence of negative resistance thus enables the bursting cell to oscillate, whereas its absence precluldes such oscillations
150 citations
TL;DR: These studies with extracellular macro-electrodes have shown that the lobster cardiac ganglion, consisting of nine cells of complex form, is capable of initiating at regular intervals complex bursts consisting of several to many impulses in each cell, and that there is a distinct pattern in the whole complex as well as in the bursts of impulse in each unit.
Abstract: With the introduction of the lobster cardiac ganglion into the service of physiology by Welsh and Maynard (1951) and Maynard (1953a—c, 1954, 1955), an extremely valuable preparation for the analysis of the properties and mechanisms of organized groups of neurones became available. Maynard has studied particularly the organization of the normal burst which initiates each heart beat and the consequences of stimulation of the extrinsic inhibitor nerve from the central nervous system, which he found to contain a single inhibitory axon on each side. These studies with extracellular macro-electrodes, partly confirmed by Matsui (1955), have shown: (a) that the ganglion, consisting of nine cells of complex form (Fig. 1 and Alexandrowicz, 1932), is capable of initiating at regular intervals complex bursts consisting of several to many impulses in each cell; (b) that there is a distinct pattern in the whole complex as well as in the bursts of impulses in each unit; and (c) that there is a division of labour among the ganglion cells. Certain of the cells apparently normally initiate the burst which represents one heart beat, others, although capable of spontaneous firing, apparently normally follow. These latter certainly, and possibly also the former, are motoneurones to the myocardium. Both are probably sensitive, but to different degrees, to stretch or inflation of the heart, in the wall of which the ganglion lies (Bullock, Cohen & Maynard, 1954), and to the effects of the extrinsic inhibitor axon and the accelerator axons, of which Maynard (1954) reported there are two. The followers are integrative as indicated by the fact that their pattern of discharge is not the same as that of any antecedent cell.
113 citations