Neuronal Circuit Mediating Escape Responses in Crayfish

The synapses between the lateral giant axon and the giant motor axon found in the abdominal ganglia of the ventral nerve cord of the crayfish Procambarus clarkii are electronic. The junctional membrane rectifies, favoring impulse transmission from lateral giant fiber to giant motor fiber. This rectifying electronic junction consists of closely apposed membranes indistinguishable from ordinary arthropod gap junctions. The apposed membranes contain intramembrane particles that are -12.5 nm in width. These particles have a central depression and are arranged in a loosely ordered array with a center-to-center spacing of about 20 nm.The only obvious morphological evidence of asymmetry is the presence of vesicles (about 80 nm in diameter) in the cytoplasm adjacent to the junctional region of the presynaptic lateral giant fiber. Vesicles are not present in the adjacent cytoplasm of the postsynaptic giant motor fiber; however, mitochondria and smooth tubular endoplasmic reticulum are more frequent in the cytoplasm of the giant motor fiber.KEY WORDS cell-to-cell communication rectifying electrotonic junction gap junction freeze-fracture -electron microscopy Although most electrotonic junctions behave as fixed resistances connecting coupled cells, a few instances are known in which the junctions rectify. Furshpan and Potter (9) established that transmission at the giant motor synapse of the crayfish is electrical with rectification. Conduction is essentially a one-way transmission from lateral giant fiber to giant motor fiber. When the potential in the lateral giant axon (presynaptic) is positive relative to the potential in the giant motor fiber t Dr. Keeter died 17 February 1976.(postsynaptic), junctional resistance is low. At rest, and when the motor fiber is more positive, junctional resistance is high. Thus orthodromic transmission is favored over antidromic.Robertson (28) and Stifling (30) have suggested that the junctional membranes in this synapse form intimate contact. Our preliminary findings (12,15) indicate that these rectifying junctions may be similar morphologically to the more common linear electrotonic synapses. To positively identify topologically the location of these junctions, nerve cords were initially prepared for scanning electron microscopy. Further studies of this synapse on both sectioned and freeze-fracture preparations were carried out. We were unable to distinguish any structural differences between the 764 J. CELL BIOLOGY 9 The Rockefeller University Press

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“…However, these additional synapses are found within the neuropil of the abdominal ganglia (16,29,32,33) and not at the site identified in Fig. 1.…”

Section: Resultsmentioning

confidence: 98%

The fine structure of a rectifying electrotonic synapse.

Hanna¹,

Keeter²,

Pappas³

1978

The Journal of Cell Biology

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“…These studies showed that one mechanism for learning and short-term memory evident in both the gill-withdrawal reflex of Aplysia and in the tail flick response of crayfish is a change in synaptic strength brought about by modulating the release of transmitter. A decrease in transmitter release is associated with short-term habituation, whereas an increase in transmitter release occurs during short-term dishabituation and sensitization (Castellucci et al, 1970;Zucker et al, 1971;Kandel, 1974, 1976) (for early reviews, see Kandel, 1976;Carew and Sahley, 1986).…”

Section: Procedural Memorymentioning

confidence: 99%

The Biology of Memory: A Forty-Year Perspective

Kandel¹

2009

J. Neurosci.

182

102

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In the forty years since the Society for Neuroscience was founded, our understanding of the biology of memory has progressed dramatically. From a historical perspective, one can discern four distinct periods of growth in neurobiological research during that time. Here I use that chronology to chart a personalized and selective course through forty years of extraordinary advances in our understanding of the biology of memory storage.Emergence of a cell biology of memory-related synaptic plasticity By 1969, we had already learned from the pioneering work of Brenda Milner that certain forms of memory were stored in the hippocampus and the medial temporal lobe. In addition, the work of Larry Squire revealed that there are two major memory systems in the brain: declarative (explicit) and procedural (implicit or nondeclarative). Declarative memory, a memory for facts and events-for people, places, and objects-requires the medial temporal lobe and the hippocampus (Scoville and Milner, 1957;Squire, 1992;Schacter and Tulving, 1994). In contrast, we knew less about procedural memory, a memory for perceptual and motor skills and other forms of nondeclarative memory that proved to involve not one but a number of brain systems: the cerebellum, the striatum, the amygdala, and in the most elementary instances, simple reflex pathways themselves. Moreover, we knew even less about the mechanisms of any form of memory storage; we did not even know whether the storage mechanisms were synaptic or nonsynaptic.In 1968, Alden Spencer and I were invited to write a perspective for Physiological Reviews, which we entitled "Cellular Neurophysiological Approaches in the Study of Learning." In it we pointed out that there was no frame of reference for studying memory because we could not yet distinguish between the two conflicting approaches to the biology of memory that had been advanced: the aggregate field approach advocated by Karl Lashley in the 1950s and Ross Adey in the 1960s, which assumed that information is stored in the bioelectric field generated by the aggregate activity of many neurons; and the cellular connectionist approach, which derived from Santiago Ramon y Cajal's idea (1894) that learning results from changes in the strength of the synapse. This idea was later renamed synaptic plasticity by Kornorski and incorporated into more refined models of learning by Hebb. We concluded our perspective by emphasizing the need to develop behavioral systems in which one could distinguish between these alternatives by relating, in a causal way, specific changes in the neuronal components of a behavior to modification of that behavior during learning and memory storage (Kandel and Spencer, 1968). Procedural memoryThe first behavioral systems to be analyzed in this manner were simple forms of learning in the context of procedural memory. From 1969 to 1979, several useful model systems emerged: the flexion reflex of cats, the eye-blink response of rabbits, and a variety of invertebrate systems: the gill-withdrawal reflex of Aplysia, olfac...

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“…Several studies have shown that with repeated activation of this afferent input, homosynaptic depression occurs at the first chemical synapse in the reflex pathway, giving rise to the hypothesis that homosynaptic depression at this synapse may provide the cellular mechanism of habituation in this system (Krasne, 1969;Zucker et al, 1971;Zucker, 1972). As recently pointed out by Krasne and Teshiba (1995), all of the experiments examining homosynaptic depression in the crayfish were carried out in acute, surgically reduced preparations that did not permit descending modulatory influences from higher brain centers to be expressed.…”

Section: Habituation In the Tail-flip Response Of Crayfishmentioning

confidence: 99%

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

Stopfer¹,

Carew

1996

J. Neurosci.

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In cellular studies of habituation, such as in the gill and siphon withdrawal reflex to tactile stimulation of the siphon of Aplysia, a mechanism that has emerged as an explanation for response decrement during habituation is homosynaptic depression at sensory neurons mediating the behavioral response. We have examined the contribution of homosynaptic depression to habituation in sensory neurons that contribute to two reflex behaviors in Aplysia, tail withdrawal and siphon withdrawal, both elicited by threshold-level tail stimulation. In a companion paper (this issue), we reported that repeated tail stimulation, identical to that producing habituation in siphon withdrawal in freely moving animals, also produces habituation in reduced preparations. In this paper, we extend these behavioral findings by showing that in reduced preparations, identical tail stimulation also produces habituation of the tail withdrawal reflex. In addition, our cellular experiments show that (1) identified sensory and motor neurons in both reflex systems respond to identical repeated tail stimulation; in sensory neurons it produces a progressive decrease in spike number and increase in spike latency, and in motor neurons it produces progressive decrement in complex EPSPs and spike output. (2) Homosynaptic depression of the tail sensory neuron to tail motor neuron synapse does occur when the sensory neurons are activated repetitively by intracellular current. (3) Homosynaptic depression at this synapse does not occur when the sensory neurons are activated repetitively by threshold-level tail stimuli that elicit the behavioral reflex and cause habituation; rather, the sensory neurons exhibit significant heterosynaptic facilitation. Thus, in these reflexes, habituation is not accompanied by homosynaptic depression at the sensory neurons, suggesting that the plasticity underlying habituation occurs primarily at interneuronal sites.

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Neuronal Circuit Mediating Escape Responses in Crayfish

Cited by 134 publications

References 20 publications

The fine structure of a rectifying electrotonic synapse.

The fine structure of a rectifying electrotonic synapse.

The Biology of Memory: A Forty-Year Perspective

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

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