Inhibitory axoaxonal and neuromuscular synapses in the crayfish opener muscle: Membrane definition and ultrastructure

Govind, C. K.; Atwood, Harold L.; Pearce, Joanne

doi:10.1002/cne.903510313

Cited by 30 publications

(34 citation statements)

References 36 publications

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“…2). In contrast, among excitatory synapses, a few synapses always lacked a dense bar in these same muscles, as reported previously for other crayfish muscles (Govind et al, 1995;King et al, 1996). The dense bar active zones of both phasic and tonic inhibitory axons to the extensor muscles were of similar length (Table 4).…”

Section: Electron Microscopysupporting

confidence: 65%

“…The latter was determined by summing the product of section thickness and synapse length (calculated using calipers preset at 2 mm) for each of the sections on which the synapse was present (Govind et al, 1995). Only fully sectioned (complete) synapses were used to calculate mean synaptic area and total synaptic area.…”

Section: Electron Microscopymentioning

confidence: 99%

“…For electron microscopy, the preparation of exposed abdominal extensor muscles was superfused with primary fixative for 30 minutes (Govind et al, 1995). The primary fixative was composed of 2.5% glutaraldehyde, 0.5% formaldehyde, 4% sucrose, and 0.1% CaCl 2 in 0.1 M sodium cacodylate buffer, pH 7.4.…”

Section: Electron Microscopymentioning

confidence: 99%

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Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Kirk

Meyer

Govind

2001

J of Comparative Neurology

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Crustacean muscles are unique in their innervation by both excitatory and inhibitory neurons; therefore, they exhibit polyneuronal and multiterminal innervation. Because excitatory motoneurons are broadly divided into phasic and tonic types, we hypothesized that inhibitory neurons would follow a similar dichotomy. The abdominal extensor muscles in crayfish are separated into parallel deep and superficial bundles; the former has fast muscle fibers innervated by phasic excitatory motoneurons, and the latter has slow fibers supplied by tonic excitatory motoneurons. Each muscle also is innervated by a single, separate inhibitory neuron that uses gamma-aminobutyric acid (GABA) as the inhibitory neurotransmitter. The pattern of axonal branching by the separate inhibitory axons in phasic and tonic abdominal extensor muscles was visualized with confocal microscopy in preparations labeled for GABA-like immunoreactivity. Initial observations indicated that the phasic muscle was covered by extensive GABAergic, filiform axon terminals, whereas innervation of the tonic muscle was comprised of more localized and varicose terminals. With quantitative analyses, we found that the phasic axon has a more highly branched nature than the tonic in first- and second-order branches. The phasic axon branches also were significantly longer than the tonic branches in the second- and third-order branches. Synaptic varicosities in the phasic branches were smaller and less frequent than those in the tonic branches. The fine structure of the inhibitory nerve terminals near synaptic contacts examined with thin-serial-section electron microscopy revealed distinct differences between the phasic system and the tonic system. The phasic terminals were smaller in cross-sectional area than the tonic terminals, and they had smaller synapses and fewer mitochondria. The presynaptic active zone dense bodies were similar in length and number between phasic and tonic synapses. However, their number per synaptic area was two-fold higher in phasic synapses compared with tonic synapses because of the smaller size of the phasic synapses. Thus, within the same neuromuscular system, inhibitory synaptic terminals revealed unique phasic and tonic identities similar to those observed for the excitatory axons.

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Section: Electron Microscopysupporting

confidence: 65%

Section: Electron Microscopymentioning

confidence: 99%

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Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Kirk

Meyer

Govind

2001

J of Comparative Neurology

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“…The criteria we have used to recognise synaptic junctions are those currently used for arthropods, namely, the presence of closely apposed, electron-dense membranes, a presynaptic electron dense body that is round or barlike and usually surrounded by clear or sometimes granular vesicles. Although the physiological confirmation that these structures are synapses is difficult in central nervous tissue, the physiologically characterised synaptic contacts between crayfish motorneurons and muscle (Govind et al, 1995) are ultrastructurally virtually identical to those found between central neurons.…”

Section: Synaptic Terminals In the Central Nervous System Of Crustaceansmentioning

confidence: 96%

Ultrastructure of the synaptic terminals of the dorsal giant serotonin‐IR neuron and deutocerebral commissure interneurons in the accessory and olfactory lobes of the crayfish

Sandeman

Watson

Sandeman

1995

J of Comparative Neurology

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The olfactory and accessory lobes in the crayfish are large spherical neuropils found on each side of its brain. The olfactory lobes receive the afferent axons of chemoreceptors that are located along the outer branches of the biramous first antennae. The accessory lobes receive a large input from interneurons whose axons lie in the deutocerebral commissure. A pair of large serotonergic neurons (the dorsal giant neurons) branch unilaterally in the accessory and olfactory lobes of each side. From physiological recordings, it has been proposed that the deutocerebral commissure interneurons synapse with elements in the accessory lobes that in turn connect to the dorsal giant neuron. It has also been proposed that the dorsal giant neuron is activated by inputs in the accessory lobe and that its output is in the olfactory lobe. This ultrastructural study tests this hypotheses by examining the polarity of synaptic terminals on dorsal giant neurons and deutocerebral interneurons that have been filled with neurobiotin. In double-labelled preparations, we found the deutocerebral interneurons to be presynaptic to elements in the accessory lobes, but none of these postsynaptic elements was identifiable as the dorsal giant neuron. The dorsal giant neurons receive many more synaptic inputs in the accessory lobes than in the olfactory lobe. Very few giant serotonin neuron output synapses were found in either lobe.

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“…Studies of presynaptic inhibition are typically not conducted at high stimulation rates to avoid muscle movement (Govind et al, 1995), but we wanted to study presynaptic inhibition at a more physiologically relevant frequency for the muscle so we used a short train of three stimuli. After the period of co-activation of both axons (arrow), the amplitude of the first EJP is significantly larger than the previous, inhibited EJP (paired t-test, P<0.001, N=6 preparations).…”

Section: Calcium Imagingmentioning

confidence: 99%

Interaction between facilitation and presynaptic inhibition at the crayfish neuromuscular junction

DeMill

Delaney

2005

Journal of Experimental Biology

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Action potential-mediated calcium (Ca) entry into excitor nerve terminal boutons during presynaptic inhibition and the effects of co-activation of the inhibitor on the kinetics of muscle contraction were studied at crayfish claw opener muscle. Inhibition reduced postsynaptic excitatory junction potentials (EJPs) below the threshold to initiate contraction. Upon cessation of inhibition, EJP amplitudes immediately increased severalfold due to the build-up of presynaptic facilitation during inhibition. Consequently, muscle contraction was initiated more rapidly after a period of inhibitor-excitor coactivation.Presynaptic inhibition reduced Ca entry into presynaptic excitor terminal boutons (range 0-50%, mean ± S.E.M.=20±1%, N=122 terminals; 12 preparations) and reduced the EJP amplitude (range 30-70%, mean ± S.E.M.=51±2%, N=27 cells). The decline in the EJP was proportional to the reduction of Ca influx raised to the power of 2.8. Since presynaptic inhibition reduces the number of Ca channels opened by an action potential, our data suggest cooperativity between Ca channel microdomains to initiate vesicle fusion at this synapse.The amount of inhibition of Ca influx into an excitor bouton was not correlated with either the distance to the closest inhibitor bouton or the main excitor branch, although slightly more inhibition was seen for excitor boutons on tertiary versus secondary branches. Unlike inhibitor axon stimulation, bath application of GABA caused inhibition of Ca influx that steadily increased from proximal to distal terminal boutons on a branch. We propose a model where presynaptic inhibition causes localized shunting of an actively propagated action potential in the vicinity of release sites, which can recover its amplitude outside the shunted region.

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Inhibitory axoaxonal and neuromuscular synapses in the crayfish opener muscle: Membrane definition and ultrastructure

Cited by 30 publications

References 36 publications

Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Ultrastructure of the synaptic terminals of the dorsal giant serotonin‐IR neuron and deutocerebral commissure interneurons in the accessory and olfactory lobes of the crayfish

Interaction between facilitation and presynaptic inhibition at the crayfish neuromuscular junction

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