Age-dependent alterations of synaptic performance and plasticity in crustacean motor systems

Age-dependent alterations of synaptic performance and plasticity in crustacean motor systems

Experimental Gerontology, Vol. 27, pp. 51~1, 1992 0531-5565/92 $5.00 + .00 Copyright © 1992 Pergamon Press plc Printed in the USA. All rights reserv...

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Experimental Gerontology, Vol. 27, pp. 51~1, 1992

0531-5565/92 $5.00 + .00 Copyright © 1992 Pergamon Press plc

Printed in the USA. All rights reserved.

AGE-DEPENDENT ALTERATIONS OF SYNAPTIC PERFORMANCE AND PLASTICITY IN CRUSTACEAN MOTOR SYSTEMS

H.L. ATWOOD Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5S 1A8

Abstract -- Age-related changes in synaptic performance and plasticity are surveyed in

crustacean neuromuscular systems. These systems are functionally differentiated into phasic and tonic types, with different attributes of synaptic function and plasticity. Conversion of phasic neuromuscular junctions to a more phasic phenotype can be brought about by altering the activity of selected neurons. This type of plasticity disappears in older animals in some motor neurons, but is retained in others. Developmental programs set constraints on the age-dependent modifications of plasticity. Crustacean motor neurons are often characterized by great longevity, with progressive addition of new branches and synapses to keep up with growth of innervated muscle cells. Certain age-related compensatory mechanisms found in neuromuscular junctions of other species may not be required in crustaceans. Key Words: crustacean, synapse, motoneuron, aging, plasticity, activity

INTRODUCTION THE MOTORSYSTEMSof decapod crustaceans provide unique opportunities for investigations of age-related effects in the nervous system, particularly those affecting mechanisms of synaptic plasticity. The peripheral motor axons to locomotory muscles are relatively few in number and large in size; hence, unique identification of individual neurons is easily accomplished. The neuromuscular synapses of individual neurons display a wide range of plasticity in synaptic transmission, representative of similar processes found among central neurons (Atwood, 1976, 1982). Of particular interest for studies in aging and development are the wide range of life spans found among decapod crustaceans, and the ability of isolated parts of neurons to survive for extended periods of time. The long life span of species such as the American lobster (Homarus americanus) provides the opportunity to study changes in single identified neurons over several decades, and to observe age-related changes in synaptic transmission and plasticity at the level of identified nerve terminals (e.g., De Rosa and Govind, 1978). The long-term survival of isolated motor nerve endings (reviewed in Bittner, 1988) affords a situation in which processes sustaining neuronal survival in adult animals can be investigated. The accessibility of identified motor nerve terminals and neuromuscular junctions in the periphery permits a range of experimental techniques to be applied with advantage. Intracel51

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lular recording of synaptic potentials, extracellular recording of quantal currents, injection of pharmacological agents into subterminal axon branches, and correlated microanatomicaL and microphysiological studies are all possible, and more readily performed in combination using crustacean motor systems than in other material. To date. a number of investigations of development, transformation, regeneration, and effects of age on synaptic performance and plasticity have been carried out in crustacean motor systems. The present review will deal mainly with the last-mentioned topic. CRUSTACEAN NEUROMUSCULAR SYSTEMS AND PLASTICITY The organizational and physiological features of crustacean neuromuscular systems have been reviewed several times (Atwood. 1976. 1982: Atwood and Wojtowicz. 1986); relevant points will be summarized only briefly here. Peripheral motor innervation consists of excitatory and inhibitory axons which act on the locomotory muscles and on each other. The axons ramify extensively within their target muscles. providing multiterminal innervation to muscle fibers. Each terminal forms a number of morphologically well-defined neuromuscular synapses, typically about 0.5-1 m 2 in contact area: many of these possess discrete "'active zones" where it is thought that release of transmitter substances occurs (reviewed in Atwood and Wojtowicz, 1976; Atwood and Govin& 1990). Current evidence suggests that there are more synapses seen at the morphological level than are needed to generate synaptic potentials, at least during low frequencies of s6mulation (e.g.. Atwood and Tse, 1988: Wojtowicz et aI., in press). Note that a sublirrfinaI population of synapses exists which may undergo recruitment under particular physiological circumstances and could account in part for short-term or long-term alterations in synaptic transmission. The different individual excitatory motor axons vary in their physiological proper6es. It has long been recognized that specialized °phasic' and 'tonic' motor axons occur° sometimes innervating the same muscle and sometimes entirely separate muscles (Kennedy and Takeda, 1965). These axons subserve different functional roles. Phasic axons produce rapid, shortlasting movements; their synapfic transmission generates large excitatory postsynaptic potentials which fatigue rapidly with repetitive stimulation. Tonic axons produce sustained or repetitive movements: their synaptic transmission generates small to intermediate-sized excitatory postsynaptic potentials (EPSPs) which are remarkably resistant to fatigue during repetitive stimulation. There are thus clear phenotypic differences between the two classes of axon. Types of synaptic plasticity encountered in these neurons are summarized in Table 1. Of particular note are the prominence of depressive effects among phasic axons, and of facilitatory effects among tomc axons, during repetitive activation, it is worth emphasizing that most of the phenomena listed (low-frequency and high-frequency depression, short- and long-term facilitation, post-tetanic potentiation) occur m isolated axons and are not dependent upon the presence of the neuronal nucleus. A different class of effect, referred to here as 'long-term adaptation,' occurs with a much slower time course (1-3 days) and requires the neuronal cell nucleus for its manifestation. To date. the phenomenon of long-term adaptation has been observed to best advantage in phasic axons (Lnenicka and Atwood 1985a,b, 1988). Probably the reason for this is that these axons normally show low rates of ongoing or spontaneous activity; they have a high threshold for recruitment in the central nervous system (Wiens, 1976). This being the case, it is easy to alter their normal activity in situ. and then to measure attributes of synaptic

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TABLE 1. IDENTIFIABLEPROCESSES OF SYNAPTIC PLASTICITYIN PHASIC AND TONIC MOTOR NEURONS OF CRUSTACEANS

Stimulation

Phasic response

Tonic response

Low-frequency stimulation (0.1-1 I-Iz)

Low-frequency depressionor little effect

No effect or slight facilitation

Intermediate frequency stimulation (5-20 Hz)

Initial facilitation, then depression

Short-term facilitation followedby long-term facilitation

High frequency stimulation, brief train (>20 Hz)

Initial facilitation, then depression

Short-term facilitation

Cessation of b r i e f train of intermediate or h i g h frequency stimulation

Posttetanic potentiation (pronounced)

Posttetanic potentiation (variable)

Intermediate frequency stimulation repeated for several days

Long-term adaptation (physiological and morphological)

Morphological changes at synapses

transmission in neurons subjected to altered activity levels. Long-term adaptation, as seen in crustacean phasic neurons, arises when the impulse activity in the neuron, or the sensory afferent activity impinging upon it, is increased (Lnenicka and Atwood, 1985b, 1988, 1989). The physiological and morphological phenotype of the 'business end' of the neuron, its neuromuscular synapses, is shifted in the tonic direction. The terminals collectively produce a smaller EPSP in the target muscle fibers, but upon repetitive stimulation this EPSP may show some degree of facilitation, and it resists depression much more effectively than the EPSP produced by the contralateral unstimulated homologue (Fig. 1). Corresponding changes in terminal morphology occur in the stimulated axon's terminals: they develop larger mitochondria and become more varicose (Lnenicka et al., 1986). The larger terminal mitochondrial volume could be linked to resistance to depression, since ongoing energy requirements may be more effectively met during prolonged activity through increased metabolic capacity. The changes start to occur 1-2 days after application of tonic stimulation; a well-developed effect, including both lowering of initial EPSP amplitude and resistance to depression, is evident 3 days after initiation of the tonic regime (Nguyen and Atwood, 1990b). Once established, the transformation persists for at least 10 days in the intact animal (Lnenicka and Atwood, 1985a). However, decreasing the neuronal activity through limb immobilization leads to the reverse changes: a larger initial EPSP and greater susceptibility to depression (Pahapill et aI., 1985). Some aspects of the mechanism of this effect have been elucidated through experimentation, The fact that adaptational changes are limited to the stimulated axon within an experi-

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FIr. 1. The effects of age on the phenomenon of long-term synaptic adaptation in synapses of the phasic motor neuron of the crayfish claw. The phasic axon was subjected to imposed tonic activity for 2 h/day at 5 Hz for 14 days. In each graph, EPSP values given are mean values from 10 fibers in five experimental claws (dotted lines) and in five contralateral control claws (solid lines . The graphs show change in EPSP amplitude when the phasic axon was stimulated steadily at 5 Hz for 30 min. (A) Results for "juvenile" crayfish, weighing approximately 3.5 gm and 6-8 months old. (B) Results for small adult crayfish, weighing approximately 11 gm and 1-2 years old. Bars for selected points represent standard errors of the mean. Adapted from Lnenicka and Atwood. 1985a. m e n t a l a n i m a l rules o u t a b l o o d - b o n e h o r m o n a l m e c h a n i s m . N e v e r t h e l e s s . h o r m o n a l factors m a y m o d u l a t e t h e e f f e c t f L n e n i c k a , 1990). I m p u l s e a c t i v i t y n e e d o n l y o c c u r w i t h i n part o f the s t i m u l a t e d a x o n a n d n e e d n o t b e p r e s e n t in t h e t e r m i n a l s t h e m s e l v e s ( L n e n i c k a a n d A t w o o d . 1988, 1989). T h i s r u l e s o u t m u s c l e a c t i v i t y a n d t r a n s m i t t e r r e l e a s e at a c t i v a t e d t e r m i nals as d e t e r m i n a n t s . A c t i v a t i o n o f the n e u r o n ' s c e n t r a l p r o c e s s e s b y a n t i d r o m i c a c t i o n p o t e n t i a l s or i n c o m i n g s e n s o r y s y n a p t i c p o t e n t i a l s s e e m s s u f f i c i e n t as a n i n d u c i n g s t i m u l u s . P r o t e i n s y n t h e s i s also m u s t b e e n a b l e d : i n h i b i t i n g it j u s t b e f o r e the p e r i o d o f t o n i c s t i m u l a -

PLASTICITY IN CRUSTACEAN SYSTEMS

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tion each day largely abolishes long-term adaptation (Nguyen and Atwood, 1990a). The most likely hypothesis for the transformation to a more tonic phenotype is that the inducing stimulus sets in motion a sequence of events which leads to protein synthesis or to utilization of a short-lived "pool" of existing proteins which have to be replaced by protein synthesis. A rapid phase of axoplasmic transport can then convey the necessary components, mitochondrial and synaptic, to the terminals. Interruption of axonal continuity abolishes the effect, indicating the requirement for axoplasmic transport (Nguyen and Atwood, 1990b). A few studies have been done on tonic neurons subjected to extra activity (Mearow and Govind, 1989) or in a state of extreme inactivity (Bittner, 1968; Acosta-Urquidi, 1978). Only morphological observations are available for a tonic neuron (opener-stretcher neuron of the crayfish) stimulated in situ. The number of presynaptic dense bars ("active zones") per unit surface area of the terminal increases. Neurons in crabs (Acosta-Urquidi, 1978) or crayfish (Bittner, 1968) kept inactive (and possibly also undernourished) for long periods show smaller EPSPs, but correlated morphological studies are not available. The results suggest that tonic axons, like phasic axons, become modified in response to altered activity levels (or other environmental factors). Hormonal and nutritional modulation of such events remains as yet unexplored.

Age-related effects Crustaceans share with other arthropods mechanisms for development and growth that are hormonally regulated and linked to the moulting cycle: Some of the larger decapods are unusual among arthropods in their longevity and in their ability to attain relatively large sizes. Studies of age-related changes in neuronal plasticity must address the possibility that such changes may be steered primarily by one of several categories of mechanism: a) genetically predetermined events; b) hormonally controlled events, especially those related to the moulting cycle; c) events related to growth in size of neurons and/or their targets of innervation; d) events related to changes in neuronal activity; e) events related to senescence. All of these categories of event are likely to be inter-related, and not cleanly separable. Work to date in crustacean material as it relates to neuronal plasticity has addressed categories c) and d), though the total amount of work is modest in comparison with that invested in vertebrates and insects. Developmental programs. Crustacean species undergo well-defined stages of development; these differ among species, but have in common a tight relationship to stages defined by periodic moults. Studies of nerve and muscle development during these early stages have been primarily morphological in nature, with some physiological observations (reviews: Govind, 1982; Govind et al., 1987). Little is known in detail of the influence of genetic programs on neuronal plasticity. It is clear from studies on claw development and differentiation in lobsters and snapping shrimp that "critical periods" exist during which neuromuscular properties can be influenced by activity (in lobsters) or by other neural influences (in snapping shrimp; Govind et al., 1987). Such neural influences, acting during a genetically permitted time window, lead to specialized claw differentiation with obligatory neuromuscular properties. Thus, once the permitted neural influence has had its effect, development proceeds in a genetically predetermined direction, resulting in the adult configuration and

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H,L. ATWOOD

properties of the neuromuscular system. The nature of the genetic programs and their regulation is almost completely unknown at present. Besides the studies devoted to production of claw asymmetry, some work has been done on alteration of peripheral innervation fields in abdominal muscles during development (Stephens and Govind, 1981; Govind et al., 1985): In the American lobster, innervation of abdominal extensor muscles by common excitatory and inhibitory neurons is more widespread in the embryo and early postembryonic stages than in |ater postembryonic stages and adults; retraction of axonal branches and synapse elimination is inferred. Another interesting example of a developmental program affecting a neuromuscular system is found in the locomotory exopodites of larval lobsters. The muscles driving these ap, pendages, and the motor neurons supplying them, undergo degeneration during larval development (Govind et al., 1988). These examples illustrate the overriding importance of the framework for neural and mus, cular development established by genetic factors. Within this framework, other factors may contribute to the properties of the nervous system. Hormonal influences. There is some evidence that hormonal conditions may influence the ability of neurons to undergo plastic changes. During limb regeneration, neuromuscular synapses formed in limb buds show physiological immaturity: failures of transmission during repetitive stimulation, large fluctuations in amplitude of EPSPs, and rapid fatigue (Govind et al., 1973). Soon after moulting has occurred, the synapses acquire more normal properties. Similar progression in physiological properties has been reported in claw muscles of lobsters during normal development (Costello et al., 1981). In small adult crayfish, preliminary observations have indicated that the activity-induced changes of long-term adaptation are greatly increased at the time of moulting (Lnenicka, 1990). The details of hormone action in such cases have not yet been established, but further work could lead to more understanding of hormone-regulated plasticity in identified crustacean neurons. Growth-related effects. Larger decapods, including crayfish and lobsters, continue to increase in size over several (or many) years Muscle fibers generally increase in length and diameter, with resultant decrease in input resistance and increase in membrane time constant (Bittner. 1968: Lnenicka and Mellon, 1983a; Mellon. 1984). These changes in muscle fibers are accompanied, in some cases, by relatively constant EPSP amplitudes. For this to occur. adjustments of the neuromuscular junctions must take place, and these have been defined by morphological and physiological studies. In the American lobster, the well-defined limb accessory flexor muscle is innervated by a single excitatory motor neuron which shows progressive branching and synaptic reorganization during growth (De Rosa and Govind. 1978: Govind and Pearce, 1981: Govind, 1982). The neuromuscular synapses increase both in number and in size as the muscle fibers ge~ larger. Correspondingly, increased quantal content is observed at individual regions of synaptic contact. An additional compensatory mechanism was discovered in slow flexor muscles of crayfish by Lnenicka and Mellon (1983a), namely, increased duration and amplitude of the quantal current. This mechanism, though insufficient by itself to maintain EPSP ampS-

PLASTICITYIN CRUSTACEANSYSTEMS

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tude in larger muscle fibers, does serve to increase the size of the quantal voltage event to a significant degree. The question of whether such compensatory changes at the synaptic level are age-related or growth-related was addressed experimentally by Lnenicka and Mellon (1983b). Growth of slow flexor muscles was retarded by interfering with their tendinous attachments. In such muscles, size constancy of the EPSP was maintained in spite of the reduced size of the target muscle fibers. Thus, the nerve terminals are responsive to the size (and resulting electrical properties) of their targets, suggesting a feedback mechanism between target and innerration. These examples illustrate that age-related growth is a possible determinant of synaptic properties and plasticity in crustacean neuromuscular systems. Activity-related factors. The ability of the phasic motor neuron of the crayfish claw closer muscle to undergo long-term adaptation in response to alterations in nem'al activity varies with the age of the animal (Fig. 1). Small adult crayfish exhibit the physiological transformation with as little as 1 or 2 days of extra activity (Nguyen and Atwood, 1990b). In contrast, larger (and older) adult specimens appear to lose this plastic ability. A possible seasonal effect on long-term adaptation has been discerned (Lnenicka, 1990). Crayfish studied during the winter are more likely to show full-blown long-term adaptation than those studied in the summer. It is possible that because of the higher level of activity in crayfish during the summer, adaptation of neurons has already occurred, and less can be produced by conventional experimental stimulation of the neuron. Age-dependent modification of plasticity appears to vary from one neuromuscular system to another. In crayfish, the phasic abdominal extensor neurons exhibit long-term adaptation in both small and large adults (Fig. 2). There is no immediate explanation for the difference between claw and abdominal neurons in this feature of adaptation; however, it can be noted that crayfish claw muscles shift increasingly to a more tonic phenotype with age (Govind and Pearce, 1985) with possible obsolescence of the phasic axon. The abdominal extensor muscles probably retain their functionality and their phasic capabilities more uniformly throughout life. Senescence. As noted above, some crustacean neuromuscular systems undergo degenerative changes, either rapid (Govind et al., 1988) or gradual (Govind and Pearce, 1985). In this, there are obvious parallels with certain neuromuscular changes in insects (Truman, 1992). Of equal interest is the remarkable ability of many crustacean motor neurons to remain functional for many years, or even for decades. The viability of isolated terminals of crustacean motor neurons suggests the existence of sustaining mechanisms which allow them to operate in partial independence from their cell bodies. Isolated terminals can survive for several months (review: Bittner, 1988). Synaptic transmission is sustained, but deteriorates with time (Velez et al., 1981; Pamas et al., 1991). Mechanisms which sustain the isolated decentralized axon include transfer of proteins and possible other materials from glial cells (Bittner, 1988) and, in some cases, incorporation of extra nuclei, possibly from adaxonal glia (Atwood et al., 1989). Thus, the age-dependent deterioration, or lack of it, in specific motor axons may be linked to changes in properties of associated glial cells, as well as changes in target muscle fibers.

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Fit. 2. Comparison of resistance to synaptic depression as a result of long-term adaptation m phasic neurons of crayfish abdominal extensor muscles for "juvenile" (A) and "adult" (B) crayfish. EPSPs were recorded from specific identified muscle fibers during stimulation of Axon 3 of the deep extensor muscles. Initial EPSP amplitudes were measured before the application of a 5 Hz train by averaging eight responses at 0.1 Hz. The axon was then stimulated at 5 Hz for 20 min, and EPSP amplitudes at the end of the train were obtained by averaging 16 responses (at 5 Hz). Results shown in A were obtained from juvenile crayfish (N = 8) that had been conditioned for 3 days. Results shown in B were obtained from adult crayfish (N - 6) that had been conditioned for 7 days. In both cases, the animals were allowed to rest for 3-4 days before EPSP amplitudes were measured. The conditioning stimulation was delivered in 1 s bursts of 5 Hz delivered every 2 s to give an average conditioning frequency of 2.5 Hz over a period of 4 h per day; thus, the same number of conditioning stimuli were applied as for Figure 1. (From Mercier and Atwood, 1989).

The decentralized axon preparation is a potentially useful tool for investigation o f m e c h a nisms o f t u r n o v e r and maintenance o f synapses.

DISCUSSION This b r i e f o v e r v i e w o f age-related changes in neuronal plasticity in crustacean neuromuscular systems illustrates several general features: 1. A general f r a m e w o r k for d e v e l o p m e n t and senescence is established through genetic regulatory m e c h a n i s m s . 2. W i t h i n this f r a m e w o r k , properties o f synapses and m u s c l e fibers m a y be influenced or determined by neuronal activity, and possibly by h o r m o n e s . 3. There appears to be coordinated regulation o f transmitter release properties of terminals, n u m b e r o f synapses, and quantal effectiveness through interactions b e t w e e n motor neurons, muscle fibers, and associated glial cells. All o f these general features can be f o u n d in other species, and in fact there are striking parallels b e t w e e n crustacean n e u r o m u s c u l a r systems and others. M a m m a l i a n n e u r o m u s c u l a r junctions, like those o f crustaceans, are differentiated into phasic and tonic types. A t tonic n e u r o m u s c u l a r junctions, e x p e r i m e n t a l l y i m p o s e d inactivity and total disuse p r o m o t e the appearance o f a m o r e tonic p h e n o t y p e (Robbins, 1980) as in crustaceans (Pahapitl et at,,

PLASTICITY IN CRUSTACEAN SYSTEMS

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1985). Some of the features of long-term adaptations have been described also in frog neuromuscular junctions subjected to extra stimulation (Hinz and Wernig, 1987). In addition, a seasonal effect on transmitter release, similar to the effect observed in crayfish, has been reported for frogs (Pawson and Grinnell, 1989). In Aplysia, some neuromuscular systems can be modified by chronic stimulation, while others are not (Peretz et al., 1982; Peretz and Srivatsan, 1992). Thus, there is good reason to believe that the general features of long-term adaptation are widespread. Age-dependence of this type of plasticity has not been studied in vertebrates, as it has in crayfish, but appears to occur in molluscs (Peretz and Srivatsan, 1992). The phenomenon of differential effects of age on synaptic performance, illustrated here in Fig. 1 and 2, is known elsewhere, for example at the mammalian neuromuscular junction (Smith, 1988) and in molluscan motor systems (Peretz et al., 1982; Peretz and Srivatsan, 1992). In crustaceans, a major theme of compensation for increased age and growth appears to be enlargement of peripheral arborizations and addition of more synapses. Other compensatory mechanisms have been uncovered elsewhere, particularly in mammals. For example, at the mammalian neuromuscular junction, transmission is maintained in older animals through increased transmitter turnover (Kelly and Robbins, 1986). Mammalian neuromuscular junctions also show morphological plasticity in the adult (Cardasis and Padykula, 1981; Fahim and Robbins, 1982; Fahim et al., 1983) but not on the same scale as in tonic motor neurons of decapod crustaceans, where the number of terminals and of individual synapses for a single neuron may increase by 1 or 2 orders of magnitude. Additional compensatory mechanisms in mammals have been discovered in the central nervous system. An example in the hippocampus is the strengthening of individual excitatory projections of the afferent perforant path to granule cells (Barnes and McNaughton, 1980) as a compensation for the decline in number of afferent synapses. Effects of this sort have not been seen to date in crustaceans. In conclusion, age-related effects on synaptic performance and plasticity occur in crustacean motor systems. Some of these can also be found in other species, but some may be uniquely emphasized in crustaceans. The ability to follow individual motor neurons through life stages representing periods of many years remains as an advantage of crustacean motor systems for studies of age-related changes and resistance to such changes. A detailed description of the remodelling of axon terminals with growth in lobsters is given by Govind (1992). REFERENCES ACOSTA-URQUIDI,J. Dormant synapsesin a crustacean neuromuscular system. Can. J. Physiol. Pharmacol. 56, 463-468, 1978. ATWOOD, H.L. Organization and synaptie physiology of crustacean neuromuscular systems. Prog. Neurobiol. 7, 291-391, 1976. ATWOOD, H.L. Synapses and neurotransmitters. In: The Biology of Crustacea. Vol. 3, Atwood, H.L. and Sandeman, D.C. (Editors), pp. 105-150, AcademicPress, New York, NY, 1982. ATWOOD, H.L., DUDEL, J., FEINSTEIN,N., and PARNAS, I. Long-termsurvival of decentralized axons and incorporation of satellite cells in motor neurons of rock lobsters. Neurosci. Lett. 101, 121-126, 1989. ATWOOD, H.L. and GOVIND, C.K. Activity-dependentand age-dependent recruitment and regulation of synapses in identified crustacean neurones. J. Exp. Biol. 153, 105-127, 1990. ATWOOD, H.L. and TSE, F.W. Changes in binomial parameters of quantal release at crustacean motor axon terminals during presynapticinhibition. J. Physiol. (Lond.) 402, 177-193, 1988.

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ATWOOD, H.L. and WOJTOWICZ, J.M. Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. Int. Rev. Neurobiol. 28, 275-362. 1986. BARNES. C.A. and McNAUGHTON, B.L. Physiological compensations for loss of afferent synapses in rat hippocampal granule cells during senescence. J. Physiol. 309, 473-485. 1980. BITTNER, G.D. The differentiation of crayfish muscle fibers during development. J. Exp. Zool. 167. 439-456. 1968. BITTNER. G.D. Long-term survival of severed distal axonal stumps in vertebrates and invertebrates. Am. Zool. 28, 1165-1179. 1988. CARDASIS, C.A. and PADYKULA. H.A. Ultrastructural evidence indicating reorganization at the neuromuscular junction in the normal rat soleus muscle. Anat. Rec. 200, 41-59. 1981 COSTELLO. W.J.. HILL. R., and LANG. F. Innervation patterns of fast and slow motor neurons during deveaopment of a lobster neuromuscular system. J. Exp. Biol. 91, 271-284. 1981. DeROSA, R.A. and GOVIND. C.K. Transmitter output increases m an identifiable lobster motoneurone with growth of its muscle fibers. Nature 273, 676-678. 1978. FAHIM. M.A. and ROBBINS, N. Ultrastructural studies of young and old mouse neuromuscular junctions. J. Neurocvtol. 11, 641-656. 1982. FAHIM, M.A.. HOLLEY, J.A., and ROBBINS. N. Scanning and light microscopic study of age changes a~. a neuromuscular junction in the mouse. J. Neurocytol. 12, 13-25. 1983. GOVIND, C.K Development of nerve, muscle and synapse. In: Biology of Crustacea. Vol. 3, Atwood, I-t.L. and Sandeman D.C. (Editors), pp. 185-204. Academic Press. New York, NY. 1982. GOVIND. C.K. Age-related remodeling of lobster neuromuscular terminals. Exp. Gerontol. 27, 63-74, 1992. GOVIND. C.K. and PEARCE. J. Remodeling of multiterminal innervation by nerve terminal sprouting in an identifiable lobster motoneuron. Science 212, 1522-1524, 1981. GOVIND. C.K. and PEARCE. J. Enhanced reappearance of fast fibers in regenerating crayfish claw closer muscles. Dev. Biol. 107. 206-212. 1985 GOVIND, C.K., ATWOOD. H.L.. and LANG. F. Synaptic differentiation in a regenerating crab-limb muscle. Proe. Natl. Acad. Sci. U. S. A. 70, 822-826, 1973. GOVIND. C.K., STEPHENS. P.J., and EtSEN. J.S. Polyneuronal innervation of an adult and embryonic ~obster muscle. J. Embryol. Exp. Morphol. 87. 13-26, 1985. GOVIND. C.K.. MELLON, D. and QUIGLEY, M.M. Muscle and muscle fiber type transformation ~n clawed crustaceans. Am. Zool. 27, 1079-1098. t987. GOVIND. C.K., KIRK, M.D.. and PEARCE. J. Highly active neuromuscular system in developing lobsters with programmed obsolescence. J. Comp. Neurol. 272, 437-449. 1988. HINZ, I. and WERNIG. A Prolonged nerve stimulation causes changes in transmitter release at the frog neuromuscular junction. J. Physiol. (Lond.)401. 557-565. 1988. KELLY. S.S. and ROBBINS. N. Sustained transmitter output by increased transmitter turnover in limb muscles of old mice. J. Neurosci. 6, 2900-2907, 1986. KENNEDY. D. and TAKEDA, K. Reflex control of abdominal flexor muscles in the crayfish. I. The twitch system. J. Exp. Biol. 43, 211-227. 1965. LNENICKA. G.A. Activity-dependent development of synaptic varicosities at terminals of an identified crayfish motoneuron. In: Activity-Driven CNS Changes in Learning and Development, State University of New York at Albany, 1990. LNENICKA. G.A. and ATWOOD. H.L. Age-dependent long-term adaptation of crayfish phasic motor axon synapses to altered activity. J. Neurosci. 5, 459-467, 1985a. LNENICKA. G.A. and ATWOOD. H.L. Long-term facilitation and long-term adaptation at synapses of a crayfish phasic motoneuron. J. Neurobiol. 16, 97-110. 1985b. LNENICKA G.A. and ATWOOD. H.L. Long-term changes in neuromuscular synapses with altered sensory input to a crayfish motoneuron. Exp. Neurol. 100, 437-447. 1988. LNENICKA. G.A. and ATWOOD. H.L. Impulse activity of a crayfish motoneuron regulates its neuromuscular synaptic properties. J. Neurophysiol. 61, 91-96, 1989. LNENICKA G.A. and MELLON, D. Changes in electrical properties and quantal current during growth of identified muscle fibres in the crayfish. J. Physiol. (Lond.) 345, 261-284, 1983a. LNENICKA. G.A. and MELLON. D. Transmitter release during normal and altered growth of identified muscle fibres in the crayfish. J. Physiol. (Lond.) 345, 285-296. 1983b. LNENICKA G.A.. ATWOOD. H.L.. and MARIN. L. Morphological transformation of synaptic terminals of a phasic motoneuron by long-term tonic stimulation J. Neurosci. 6, 2252-2258. 1986.

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