Release properties of individual presynaptic boutons expressed during homosynaptic depression and heterosynaptic facilitation of the Aplysia sensorimotor synapse

Malkinson, Guy; Spira, Micha Ε.

doi:10.3389/fncel.2013.00165

Cited by 8 publications

(16 citation statements)

References 52 publications

(73 reference statements)

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“…The functional changes include a reduction in silent synapses and an increase in miniature EPSP (mEPSP) frequency Jin et al, 2012). HSD is primarily produced by a reduction in release probability and a disruption of excitation-secretion coupling at presynaptic varicosities, resulting in the silencing of release sites with low release probability (Eliot et al, 1994;Armitage and Siegelbaum, 1998;Royer et al, 2000;Gover et al, 2002;Zhao and Klein, 2002;Malkinson and Spira, 2013). Thus, it was somewhat surprising that the kinetics of HSD was unaffected at synapses expressing P-LTF, where release probability and mEPSP frequency are high.…”

Section: Discussionmentioning

confidence: 99%

“…Structural and functional changes at identified presynaptic sensory neurons and postsynaptic motor neurons contribute to P-LTF and to long-term sensitization of defensive withdrawal reflexes (Frost et al, 1985;Bailey and Chen, 1988;Glanzman et al, 1990;Trudeau and Castellucci, 1995;Mauelshagen et al, 1996Mauelshagen et al, , 1998Zhu et al, 1997;Hatada et al, 2000;Sherff and Carew, 2002;Wainwright et al, 2002;Cai et al, 2008;. The gill-siphon withdrawal behavior and sensorimotor synapses express bidirectional plasticity lasting minutes to weeks that reflect the nature, number, and temporal pattern of the stimuli (Pinsker et al, 1973;Castellucci et al, 1978;Montarolo et al, 1986Montarolo et al, , 1988Dale et al, 1988;Bailey et al, 1992;Zhang et al, 1994;Sutton et al, 2002;Sharma et al, 2003;Hu et al, 2011;Liu et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Persistent Long-Term Facilitation at an Identified Synapse Becomes Labile with Activation of Short-Term Heterosynaptic Plasticity

Schacher

2014

J. Neurosci.

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Short-term and long-term synaptic plasticity are cellular correlates of learning and memory of different durations. Little is known, however, how these two forms of plasticity interact at the same synaptic connection. We examined the reciprocal impact of short-term heterosynaptic or homosynaptic plasticity at sensorimotor synapses of Aplysia in cell culture when expressing persistent long-term facilitation (P-LTF) evoked by serotonin [5-hydroxytryptamine (5-HT)]. Short-term heterosynaptic plasticity induced by 5-HT (facilitation) or the neuropeptide FMRFa (depression) and short-term homosynaptic plasticity induced by tetanus [post-tetanic potentiation (PTP)] or low-frequency stimulation [homosynaptic depression (HSD)] of the sensory neuron were expressed in both control synapses and synapses expressing P-LTF in the absence or presence of protein synthesis inhibitors. All forms of short-term plasticity failed to significantly affect ongoing P-LTF in the absence of protein synthesis inhibitors. However, P-LTF reversed to control levels when either 5-HT or FMRFa was applied in the presence of rapamycin. In contrast, P-LTF was unaffected when either PTP or HSD was evoked in the presence of either rapamycin or anisomycin. These results indicate that synapses expressing persistent plasticity acquire a "new" baseline and functionally express short-term changes as naive synapses, but the new baseline becomes labile following selective activations-heterosynaptic stimuli that evoke opposite forms of plasticity-such that when presented in the presence of protein synthesis inhibitors produce a rapid reversal of the persistent plasticity. Activity-selective induction of a labile state at synapses expressing persistent plasticity may facilitate the development of therapies for reversing inappropriate memories.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Persistent Long-Term Facilitation at an Identified Synapse Becomes Labile with Activation of Short-Term Heterosynaptic Plasticity

Schacher

2014

J. Neurosci.

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“…For example, responsiveness within the first two trials could predict the subsequent pattern of habituation before adaptation was in effect. In general, although short-term habituation is correlated with failures of sensory transmission (Malkinson and Spira, 2013 ), longer term habituation cannot be reduced to either receptor adaptation or a depression of the sensorimotor synapses, presenting prima facie evidence for experience dependent change in the likelihood of responding to the same stimulus (Glanzman, 2009 ).…”

Section: Modulation Of Distal Stimulus Processing By Proximal Inputs mentioning

confidence: 99%

Habituation, sensitization, and Pavlovian conditioning

Çevik

2014

Front. Integr. Neurosci.

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In this brief review, I argue that the impact of a stimulus on behavioral control increase as the distance of the stimulus to the body decreases. Habituation, i.e., decrement in response intensity repetition of the triggering stimulus, is the default state for sensory processing, and the likelihood of habituation is higher for distal stimuli. Sensitization, i.e., increment in response intensity upon stimulus repetition, occurs in a state dependent manner for proximal stimuli that make direct contact with the body. In Pavlovian conditioning paradigms, the unconditioned stimulus (US) is always a more proximal stimulus than the conditioned stimulus (CS). The mechanisms of associative and non-associative learning are not independent. CS−US pairings lead to formation of associations if sensitizing modulation from a proximal US prevents the habituation for a distal anticipatory CS.

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“…Pioneering work using calcium indicator dyes showed that excitatory post-synaptic calcium transients (EPSCaTs), mediated mainly by calcium flowing through calcium-permeable AMPA receptors, can be used to localize and measure the strength at synapses in Aplysia sensory-motor neuron cultures (Malkinson and Spira 2010;Malkinson and Spira 2013). However, calcium dyes tend to compartmentalize over time (Paredes et al 2008), making multiday use problematic.…”

Section: Generation Of a Calcium Sensor Optimized For Visualizing Synmentioning

confidence: 99%

“…indicator dyes (Malkinson and Spira 2010;Malkinson and Spira 2013). To determine the extent to which this affected synaptic transmission, we measured the effect of this high calcium recording saline on the amplitude of the PSP.…”

Section: Src-gcamp6s Is Effective At Measuring Action Potential Evokementioning

confidence: 99%

Excitatory postsynaptic calcium transients at Aplysia sensory-motor neuron synapses allow for quantal examination of synaptic strength over multiple days in culture

Dunn

Sossin

2021

Preprint

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The ability to monitor changes in strength at individual synaptic contacts is required to test the hypothesis that specialized synapses maintain changes in synaptic strength that underlie memory. Measuring excitatory post-synaptic calcium transients through calcium permeable AMPA receptors is one way to monitor synaptic strength at individual synaptic contacts. Using a membrane targeted genetic calcium sensor, we demonstrate that one can measure synaptic events at individual synaptic contacts in Aplysia sensory-motor neuron synapses. These results show that synaptic strength is not evenly distributed between all contacts in these cultures, but dominated by multiquantal sites of synaptic contact. The probability, quantal size and quantal content can be measured over days at individual synaptic contacts using this technique. Surprisingly, most synaptic contacts were not found opposite presynaptic varicosities, but instead at areas of pre- and post-synaptic contact with no visible thickening of membranes. This technique shows promise in being able to address whether specialized synapses maintain synaptic strength underlying memory.

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Release properties of individual presynaptic boutons expressed during homosynaptic depression and heterosynaptic facilitation of the Aplysia sensorimotor synapse

Cited by 8 publications

References 52 publications

Persistent Long-Term Facilitation at an Identified Synapse Becomes Labile with Activation of Short-Term Heterosynaptic Plasticity

Persistent Long-Term Facilitation at an Identified Synapse Becomes Labile with Activation of Short-Term Heterosynaptic Plasticity

Habituation, sensitization, and Pavlovian conditioning

Excitatory postsynaptic calcium transients at Aplysia sensory-motor neuron synapses allow for quantal examination of synaptic strength over multiple days in culture

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