Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer atAplysiaSensorimotor Synapses: Empirical and Computational Analyses

Abstract

The Aplysia sensorimotor synapse is a key site of plasticity for several simple forms of learning. Plasticity of this synapse has been extensively studied, albeit primarily with individual action potentials elicited at low frequencies. Yet, the mechanosensory neurons fire high-frequency bursts in response to even moderate tactile stimuli delivered to the skin. In the present study, we extend this analysis to show that sensory neurons also fire bursts in the range of 1-60 Hz in response to electrical stimuli similar to those used in behavioral studies of sensitization. Intracellular stimulation of sensory neurons to fire a burst of action potentials at 10 Hz for 1 sec led to significant homosynaptic depression of postsynaptic responses. The depression was transient and fully recovered within 10 min. During the burst, the steady-state depressed phase of the postsynaptic response, which was only 20% of the initial EPSP of the burst, still contributed to firing the motor neuron. To explore the functional contribution of transient homosynaptic depression to the response of the motor neuron, computer simulations of the sensorimotor synapse with and without depression were compared. Depression allowed the motor neuron to produce graded responses over a wide range of presynaptic input strength. In addition, enhancement of synaptic transmission throughout a burst increased motor neuron output substantially more than did preferential enhancement of the initial phase of a burst. Thus, synaptic depression increased the dynamic range of the sensorimotor synapse and can, in principle, have a profound effect on information processing.

Long-Term Sensitization Training Produces Spike Narrowing inAplysiaSensory Neurons

“…Tail stimulation was similar to what is generally used to elicit weak withdrawal responses (Scholz and Byrne, 1987;Goldsmith and Byrne, 1993;Cleary et al, 1998;Sutton et al, 2001;Wainwright et al, 2002Wainwright et al, , 2004Antzoulatos et al, 2006). As also reported previously (Phares et al, 2003), the spiking responses to cutaneous AC (60 Hz) stimuli had short latency, were time-locked to the AC stimulus, and included high-frequency firing (approaching 60 Hz), sometimes followed by a highly variable afterdischarge. The initial response to a 5 mA, 20 ms AC stimulus (1.2 cycles) included either single or double spikes.…”

“…The synaptic stimulation procedures have been described previously in detail (Phares et al, 2003). Briefly, sensory neurons in the ventrocaudal cluster of the pleural ganglion were impaled with a single electrode (10 -15 M⍀), whereas postsynaptic motor neurons in the pedal ganglion were impaled with two electrodes: one to record membrane potential and another to inject current.…”

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).…”

“…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).…”

Burst-Induced Anti-Hebbian Depression Acts through Short-Term Synaptic Dynamics to Cancel Redundant Sensory Signals

“…Such analyses might also shed light on the more general relation between diverse underlying cellular mechanisms and the functional effects of different LTD rules on information transfer in neural networks (Egger et al, 1999;Phares et al, 2003;Birtoli and Ulrich, 2004;Tzounopoulos et al, 2004Tzounopoulos et al, , 2007Letzkus et al, 2006;Caporale and Dan, 2008).…”