Organization of synaptic inputs to paracerebral feeding command interneurons of Pleurobranchaea californica. I. Excitatory inputs

1983 ◽  
Vol 49 (6) ◽  
pp. 1517-1538 ◽  
Author(s):  
M. P. Kovac ◽  
W. J. Davis ◽  
E. M. Matera ◽  
R. P. Croll

Neurons presynaptic to the phasic paracerebral feeding command interneurons (PCP's; Ref. 55) of Pleurobranchaea were located in the isolated central nervous system (CNS) and studied anatomically by lucifer yellow injection and physiologically by current injection and intracellular recording in normal and ion-substituted seawater during quiescence and fictive feeding. The present paper describes excitatory inputs to PCP's, while the accompanying paper (54) reports inhibitory inputs. Monosynaptic excitors (MSEs) are a group of at least three monopolar neurons per hemiganglion. Two have similar dendritic structures and functional effects. Each MSE monosynaptically excites the PCP's and fires action-potential bursts in phase with PCP bursts during fictive feeding. The class I electrotonic neuron (ETI) is a single, identified monopolar neuron per hemiganglion with a sparse dendritic arborization and no descending axon in the cerebrobuccal connective (CBC). The ETI is coupled with PCP's only by means of a non-rectifying electrical synapse. Paradoxically, ETI receives opposite synaptic inputs from PCP's and fires in antiphase with PCP's during fictive feeding. Class II electrotonic neurons (ETII's) are a group of at least two identified multipolar neurons per hemiganglion with indistinguishable dendritic architectures and similar but distinguishable functional effects. Each cell is coupled with PCP's by means of a nonrectifying electrical synapse. One of the ETII's also delivers graded, long-latency poly-synaptic chemical inputs to PCP's. ETII's have descending axons in the CBC, elicit fictive feeding when depolarized, and fire cyclically and in phase with PCP's during fictive feeding. Polysynaptic excitors (PSEs) are a group of at least two identified monopolar neurons per hemiganglion with similar elaborate dendritic fields and functional effects. Each cell excites PCP's by a long-latency, relatively nongraded polysynaptic pathway. PSEs also have descending axons in the ipsilateral CBC, elicit fictive feeding when depolarized, and fire in phase with PCP's during fictive feeding. PSEs and ETII's are here recognized as subclasses of neurons previously identified as paracerebral neurons. They are inhibited by the same neurons that supply recurrent inhibition to PCP's (47), share excitatory inputs with PCP's, and exhibit a similar "command" capacity. This study thus documents redundancy and functional specialization within a command system controlling a relatively complex rhythmic motor behavior.

1984 ◽  
Vol 110 (1) ◽  
pp. 1-15
Author(s):  
W. J. Davis ◽  
M. P. Kovac ◽  
R. P. Croll ◽  
E. M. Matera

Tonic (d.c.) intracellular depolarization of the previously identified phasic paracerebral feeding command interneurones (PCps) in the brain of the carnivorous gastropod Pleurobranchaea causes oscillatory neural activity in the brain, both before and after transecting the cerebrobuccal connectives. Therefore, cycle-by-cycle ascending input from the buccal ganglion is not essential to cyclic brain activity. Instead the brain contains an independent neural oscillator(s), in addition to the oscillator(s) demonstrated previously in the buccal ganglion (Davis et al. 1973). Transection of the cerebrobuccal connectives immediately reduces the previously demonstrated (Kovac, Davis, Matera & Croll, 1983) long-latency polysynaptic excitation of the PCps by the polysynaptic excitors (PSEs) of the PCps. Therefore polysynaptic excitation of the PCps by the PSEs is mediated by an ascending neurone(s) from the buccal ganglion. The capacity of feeding command interneurones to induce neural oscillation in the isolated brain declines to near zero within 1 h after transection of the cerebrobuccal connectives, suggesting that this capacity is normally maintained by ascending information from the buccal ganglion. The results show that this motor system conforms to a widely applicable general model of the neural control of rhythmic behaviour, by which independent neural oscillators distributed widely in the central nervous system are coupled together to produce coordinated movement.


The acetylcholine-synthesizing neurons of the rabbit retina were selectively stained by intraocular injection of the fluorescent dye 4, 6-diamidino-2-phenylindole (DAP1). Retinas were then isolated from the eye, fixed for 10-30 min with 4% paraformaldehyde, and mounted flat on the stage of a fluorescence microscope. The acetylcholine-synthesizing cells were penetrated under visual control by microelectrodes filled with lucifer yellow CH. When the dye was electrophoretically injected into the cells, complete filling of their dendrites often occurred. Cells were successfully injected as long as one month after fixation of the tissue. Complete or nearly complete filling of 281 cells was accomplished, at retinal locations systematically covering the retinal surface. The cells stained with DAPI were found to form a single morphological population. They have two to seven primary dendrites, which branch repeatedly within a narrow plane and form a round or slightly oval dendritic tree. The branching becomes very fine for the distal one third of the dendritic tree, and the dendrites there are studded with small swellings. The distal dendritic tree lies mainly within one of the two thin strata of the inner plexiform layer where acetylcholine is present. The shape and size of the dendritic tree are continuously graded across the retina ; the dendritic tree is narrower and the branching denser in the central retina, wider and sparser in the periphery. From knowledge of the population density and the shape of the neurons, one can reconstruct the array of dendrites that exists within the inner plexiform layer. The overlap of the dendritic fields is an order of magnitude greater than of any other retinal neuron previously described. Because the cells not only overlap widely but branch quite profusely, a very dense plexus of cholinergic dendrites is created.


1994 ◽  
Vol 11 (3) ◽  
pp. 549-560 ◽  
Author(s):  
Stephen L. Mills ◽  
Stephen C. Massey

AbstractBoth A- and B-type horizontal cells in the rabbit retina were labeled by brief in vitro incubations of the isolated retina in the blue fluorescent dye 4,6–diamino-2–phenylindole. Intracellular injection of Lucifer Yellow into the somata revealed the morphology of the individual cells. Dye-coupling with Lucifer Yellow was seen only between A-type horizontal cells. By contrast, injection of the tracer Neurobiotin showed dye-coupling between both A- and B-type horizontal cells. There also appeared to be coupling between the axon terminals of B-type horizontal cells.The extensive dye-coupling seen following injection of Neurobiotin into a single horizontal cell soma can be used to obtain population counts of each cell type. Staining of large numbers of each cell type across the retina showed that each type increased in number and declined in dendritic diameter as the visual streak was approached, such that relatively constant coverage across the retina was maintained. In the visual streak, A-type horizontal cells numbered 555 cells/mm2 and averaged 120 μm in diameter, compared to 1375 cells/mm2 and 100 μm for B-type horizontal cells. In the periphery, the A- and B-types numbered 250 cells/mm2 and 400 cells/mm2, respectively. The average diameters of the dendritic trees at these locations were 225 μm for the A-type and 175 μm for the B-type. Coverage across the retina averaged almost six for A-type horizontal cells and 8–10 for the B-type. A-type horizontal cells in the visual streak whose elliptical dendritic fields were shown by Bloomfield (1992) to correlate physiologically with orientation bias were shown to be dye-coupled to cells with symmetrical dendritic fields.


1990 ◽  
Vol 95 (4) ◽  
pp. 755-770 ◽  
Author(s):  
G Maguire ◽  
P Lukasiewicz ◽  
F Werblin

We have correlated the membrane properties and synaptic inputs of interplexiform cells (IPCs) with their morphology using whole-cell patch-clamp and Lucifer yellow staining in retinal slices. Three morphological types were identified: (a) a bistratified IPC with descending processes ramifying in both sublaminas a and b of the inner plexiform layer (IPL), and an ascending process that branched in the outer plexiform layer (OPL) and originated from the soma, (b) another bistratified IPC with descending processes ramifying in both sublaminas a and b, and an ascending process that branched in the OPL and originated directly from IPC processes in the IPL, and (c) a monostratified IPC with a descending process ramifying over large lateral extents within the most distal stratum of the IPL, and sending an ascending process to the OPL with little branching. Similar voltage-gated currents were measured in all three types including: (a) a transient inward sodium current, (b) an outward potassium current, and (c) an L-type calcium current. All cells generated multiple spikes with frequency increasing monotonically with the magnitude of injected current. The IPCs that send their descending processes into both sublaminas of the IPL (bistratified) receive excitatory synaptic inputs at both light ON and OFF that decay with a time constant of approximately 1.3 s. Slowly decaying excitation at both ON and OFF suggests that bistratified IPCs may spike continuously in the presence of a dynamic visual environment.


1984 ◽  
Vol 113 (1) ◽  
pp. 423-446
Author(s):  
J. A. London ◽  
R. Gillette

The paracerebral neurones (PCNs) of the brain of Pleurobranchaea californica serve a command role in the initiation of feeding behaviour (Gillette, Kovac & Davis, 1978). The PCNs are synaptically excited by food stimuli applied to the oral veil of hungry, naive animals. In food avoidance-conditioned animals, the PCNs are inhibited by a barrage of inhibitory postsynaptic potentials concomitant with the suppression of feeding (Davis & Gillette, 1978). In this paper, an interneuronal pathway is described which causes inhibition of the PCNs and potentially mediates the effects of learning. The inhibitory pathway consists of three serially connected interneurones. One population, designated the Interneurone 1s (Int-1s), monosynaptically inhibits the PCNs. A second population, the Interneurone 2s (Int-2s), excites the Int-1 population. They also excite other neurones of the brain including the metacerebral giant neurones. A third population, the Interneurone 3s (Int-3s), monosynaptically excites the Interneurone 2 population. Dual intracellular recordings and current injection show that ipsilateral members of the Int-2 population are electrically coupled via a nonrectifying connection. Contralateral members of the Int-2 population are excitatorily coupled via a polysynaptic pathway. The Int-1 population is phasically active during the rhythmic motor activity that underlies feeding. In the isolated nervous system Int-1 activity is phase-locked with rhythmic PCN activity; Int-1 activity occurs maximally at the end of a PCN burst, during the retraction phase of the cycle. Int-2 activity also occurs during the retraction phase. During actual feeding in the whole animal preparation, the Int-2s are also phasically active; maximal excitation occurs during buccal mass retraction and maximal inhibition during protraction and the bite. Stimulated activity in a single Int-2 can entirely suppress the rhythmic motor activity of the feeding network evoked by electrical stimulation of the stomatogastric nerve. The suppressant effects of Int-2 activity must be mediated widely within the feeding network because the rhythmic motor output so driven is not dependent on PCN spiking. Application of an appetitive chemosensory stimulus to whole and semi-intact animal preparations initiated feeding and elicited excitation of the Int-1 and Int-2 populations. Noxious chemosensory stimuli, such as a dilute soap solution or ethanol, elicited oral veil withdrawal and inhibition of the Int-2s by multiple inhibitory postsynaptic potentials.(ABSTRACT TRUNCATED AT 400 WORDS)


2002 ◽  
Vol 87 (1) ◽  
pp. 538-547 ◽  
Author(s):  
Tiaza Bem ◽  
Yves Le Feuvre ◽  
John Simmers ◽  
Pierre Meyrand

Electrical coupling is widespread in developing nervous systems and plays a major role in circuit formation and patterning of activity. In most reported cases, such coupling between rhythmogenic neurons tends to synchronize and enhance their oscillatory behavior, thereby producing monophasic rhythmic output. However, in many adult networks, such as those responsible for rhythmic motor behavior, oscillatory neurons are linked by synaptic inhibition to produce rhythmic output with multiple phases. The question then arises whether such networks are still able to generate multiphasic output in the early stage of development when electrical coupling is abundant. A suitable model for addressing this issue is the lobster stomatogastric nervous system (STNS). In the adult animal, the STNS consists of three discrete neural networks that are comprised of oscillatory neurons interconnected by reciprocal inhibition. These networks generate three distinct rhythmic motor patterns with large amplitude neuronal oscillations. By contrast, in the embryo the same neuronal population expresses a single multiphasic rhythm with small-amplitude oscillations. Recent findings have revealed that adult-like network properties are already present early in the embryonic system but are masked by an as yet unknown mechanism. Here we use computer simulation to test whether extensive electrical coupling may be involved in masking adult-like properties in the embryonic STNS. Our basic model consists of three different adult-like STNS networks that are built of relaxation oscillators interconnected by reciprocal synaptic inhibition. Individual model cells generate slow membrane potential oscillations without action potentials. The introduction of widespread electrical coupling between members of these networks dampens oscillation amplitudes and, at moderate coupling strengths, may coordinate neuronal activity into a single rhythm with different phases, which is strongly reminiscent of embryonic STNS output. With a further increase in coupling strength, the system reaches one of two final states depending on the relative contribution of inhibition and inherent oscillatory properties within the networks: either fully synchronized and dampened oscillations, or a complete collapse of activity. Our simulations indicate that, beginning from either of these two states, the emergence of distinct adult networks during maturation may arise from a developmental decrease in electrical coupling that unmasks preexisting adult-like network properties.


1993 ◽  
Vol 10 (2) ◽  
pp. 287-295 ◽  
Author(s):  
Haohua Qian ◽  
Robert Paul Malchow ◽  
Harris Ripps

AbstractWhole-cell voltage-clamp recordings were used to examine the unusual pharmacological properties of the electrical coupling between rod-driven horizontal cells in skate retina as revealed previously by receptive-field measurements (Qian & Ripps, 1992). The junctional resistance was measured in electrically coupled cell pairs that had been enzymatically isolated and maintained in culture; the typical value was about 19.92 MΩ(n = 45), more than an order of magnitude lower than the nonjunctional membrane resistance. These data and the intercellular spread of the fluorescent dye Lucifer Yellow provide a good indication that skate horizontal cells are well coupled. The junctional conductance between cells was not modulated by the neurotransmitters dopamine (200 μM) or GABA (1 mM), nor was it affected by the membrane-permeable analogues of cAMP or cGMP, or the adenylate cyclase activator, forskolin. Although resistant to agents that have been reported to alter horizontal-cell coupling in cone-driven horizontal cells, the junctional conductance between paired horizontal cells of skate was greatly reduced by the application of 20 mM acetate, which is known to effectively reduce intracellular pH. Together with the results obtained in situ on the receptive-field properties of skate horizontal cells, these findings indicate that the gap-junctional properties of rod-driven horizontal cells of the skate are fundamentally different from those of cone-driven horizontal cells in other species. This raises the possibility that there is more than one class of electrical synapse on vertebrate horizontal cells.


1992 ◽  
Vol 67 (4) ◽  
pp. 829-840 ◽  
Author(s):  
H. G. Kim ◽  
R. F. Miller

1. Horizontal cells (HCs) of the mudpuppy (Necturus maculosus) retina were physiologically characterized with the use of intracellular recordings in a superfused, dark-adapted, retina-eyecup preparation. 2. Physiological analysis included an evaluation of rod versus cone input and a determination of the receptive field size with the use of a displaced slit of light. 3. The morphology of HCs was established through intracellular staining with horseradish peroxidase (HRP) and Lucifer yellow mixed in a single electrode. 4. Three types of horizontal cells were identified, each associated with a distinct morphology. Physiological subtypes included luminosity (L) and chromaticity (C) cells. Morphological diversities included single axon-bearing, multiple axon-bearing and, nonaxon-bearing cells. All C-type HCs lacked axons. 5. Approximately 90% of HCs encountered in this study were L-type cells, which received sign-conserving inputs from both rods and cones. These cell types contained one or more long axons that often stretched greater than 500 microns. This group was morphologically diverse, particularly with respect to variations in the number of axons, but we were unable to correlate this diversity with any unique set of physiological properties. 6. Several C-type HCs were identified (n = 8). These cells depolarized to a low-intensity, short-wavelength (SW) stimulus, whereas they hyperpolarized to high-intensity, long-wavelength stimuli. Morphologically, these cells were axonless (n = 4), with relatively small dendritic fields. 7. A third group of HCs were classified as "short wavelength preferring" HCs (n = 7). These cells responded better to a SW stimulus at all intensity levels. They were thus dissimilar to the common L-type HCs, which showed an apparent rod to cone transition as the stimulus intensity increased, suggestive of a shift from rod to cone preference. Morphologically, these cells were axonless (n = 2), but had broader dendritic fields than the C-type HCs. 8. Our observations indicate that the horizontal cell population of the mudpuppy retina is considerably more complex than previously supposed. The existence of both axon-bearing and axonless HCs, which could be correlated with L- and C-type physiology, implies that HCs may support more than one function in outer retina processing.


Sign in / Sign up

Export Citation Format

Share Document