Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica

Abstract

1. Repeated stimulation of the siphon skin results in short-term habituation of the reflex contractions of the gill (38). The habituation, in turn, is correlated with a depression of the excitatory postsynaptic potentials (EPSPs) in motor neurons from mechanoreceptor sensory neurons (SN) (7, 16). The present study was undertaken to examine the parametric features of the synaptic depression and gain insights into the mechanisms underlying the reduced transmitter release. 2. Single sensory neuron action potentials were repeatedly elicited with depolarizing current pulses while the amplitude of the resultant EPSPs in the motor neuron was monitored. Synaptic depression varies as a complex function of interstimulus interval (ISI). At an ISI of 1 s, depression is rapid and reaches a plateau at 36% of control. In contrast, the depression at an ISI of 100 s is less pronounced, showing a gradual decay to 65% of control with the 10th EPSP. Surprisingly, there are no significant differences in time course or magnitude of depression across a broad range of intermediate ISIs (3, 10, and 30 s), although depression at these ISIs is intermediate between the 1 and 100 s ISIs. 3. There is also a complex relationship between spike interval and the depression of the second of two EPSPs. Thus, depression of the second of two EPSPs or depression of a train of EPSPs is not a monotonic function of spike interval. Indeed, the data suggest that there may be a slight underlying facilitatory process with short spike intervals. 4. The results also indicate that the recovery of synaptic depression following a train of 10 stimuli is not constant. Shorter spike intervals produce more rapid recovery. 5. These data are inconsistent with a classical depletion model (33) for synaptic depression and indicate that either a single complex function of time and ISI or multiple functions underlie synaptic depression and its recovery at the sensory neuron synapse.

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

“…From this perspective, the sensory neurons are thought to release progressively less transmitter with each successive stimulus, thereby contributing progressively less input to interneurons and motor neurons mediating the behavior (Krasne, 1969;Castellucci et al, 1970;Zucker, 1972;Castellucci and Kandel, 1974;Hawkins et al, 1993). The capacity of sensory neurons to exhibit homosynaptic depression is well documented in Aplysia and other preparations (Krasne, 1969;Castellucci et al, 1970;Zucker, 1972;Klein et al, 1980;Byrne, 1982); however, the role of homosynaptic depression in mediating the behavioral decrement of habituation has been studied only in the gill and siphon withdrawal reflex elicited by siphon stimulation.…”

“…Many studies have shown that repeated, direct intracellular activation of these cells reliably causes progressive depression of excitatory synaptic transmission Klein et al, 1980;Byrne, 1982;Walters et al, 1983;Hawkins et al, 1987;Buonomano et al, 1992;Goldsmith and Byrne, 1993). Moreover, several studies in Aplysia have demonstrated habituation in behaving animals and in reduced preparations Pinsker et al, 1970;Carew et al, 1972;Stopfer and Carew, 1987); however, the role of sensory neuron homosynaptic depression in producing habituation in Aplysia so far has been examined only in the siphon-elicited gill and siphon withdrawal reflex Carew et al, 1971;Castellucci et al, 1978;Hawkins and Frost, 1995).…”

Switching Off and On of Synaptic Sites atAplysiaSensorimotor Synapses

“…The only failure of the model to closely fit the observed responses occurred when the rest was 10 sec or less (Fig. 9A), presumably because frequency facilitation was recruited at the short interstimulus intervals (Byrne, 1982;Eliot et al, 1994). Of particular significance is the fact that both the initial rapid phase of depression and the subsequent slow phase were well fit using this model, indicating that the combination of recovery between stimuli at some sites and the putative switching process can account for all aspects of synaptic depression and that it is not necessary to invoke two separate depression processes to account for the dual time course of depression.…”

Desensitization of Postsynaptic Glutamate Receptors Contributes to High-Frequency Homosynaptic Depression of Aplysia Sensorimotor Connections

“…Stimuli sufficient to elicit withdrawal reflexes evoke a high-frequency burst of spikes in the SNs (Byrne et al 1978a,b;Walters et al 1983;Stopfer and Carew 1996;Frost et al 1997;Antonov et al 1999;Phares et al 2003). Such bursts of SN activity induce homosynaptic depression of the sensorimotor synapses, a mechanism that limits the response of MNs to peripheral stimuli (Byrne et al 1978b;Walters et al 1983;Stopfer and Carew 1996;Antonov et al 1999;Phares et al 2003).For the past thirty years, homosynaptic depression of Aplysia sensorimotor synapses has been attributed exclusively to presynaptic mechanisms Byrne 1982;Gingrich and Byrne 1985;Bailey and Chen 1988;Eliot et al 1994;Armitage and Siegelbaum 1998;Royer et al 2000;Gover et al 2002;Zhao and Klein 2002). Moreover, it has been repeatedly suggested that homosynaptic depression of the sensorimotor synapse does not have a postsynaptic contribution Armitage and Siegelbaum 1998;Royer et al 2000).…”

“…For the past thirty years, homosynaptic depression of Aplysia sensorimotor synapses has been attributed exclusively to presynaptic mechanisms Byrne 1982;Gingrich and Byrne 1985;Bailey and Chen 1988;Eliot et al 1994;Armitage and Siegelbaum 1998;Royer et al 2000;Gover et al 2002;Zhao and Klein 2002). Moreover, it has been repeatedly suggested that homosynaptic depression of the sensorimotor synapse does not have a postsynaptic contribution Armitage and Siegelbaum 1998;Royer et al 2000).…”