Abstract
The retinotectal projection in Xenopus laevis has been shown to exhibit correlation-based refinement of both anatomical and functional connectivity during development. Spike timing-dependent plasticity (STDP) is an appealing experimental model for correlation-based synaptic plasticity because, in contrast to plasticity induction paradigms using tetanic stimulation or sustained postsynaptic depolarization, its induction protocol more closely resembles natural physiological activity. In Xenopus tadpoles, where anatomical remodeling has been reported throughout much of the life of the animal, in vivo retinotectal STDP has only been examined under a limited set of experimental conditions. Using perforated-patch recordings of retina-evoked EPSCs in tectal neurons, we confirmed that repeatedly driving a retinotectal EPSP 5–10 ms prior to inducing an action potential in the postsynaptic cell, reliably produced timing-dependent long-term potentiation (t-LTP) of the retinotectal synapse in young wild type tadpoles (stages 41–44). At these stages, retinotectal timing-dependent long-term depression (t-LTD) also could be induced by evoking an EPSP to arrive 5–10 ms after an action potential in the tectal cell. However, retinotectal STDP using this standard protocol was limited to a developmental sensitive period, as we were unable to induce t-LTP or t-LTD after stage 44. Surprisingly, this STDP protocol also failed to induce reliable STDP in albino tadpoles at the early ages when it was effective in wild type pigmented animals. Nonetheless, low-frequency flashes to the eye produced a robust NMDA receptor-dependent retinotectal LTD in stage 47 albino tadpoles, demonstrating that the retinotectal synapse can nonetheless be modified in these animals using different plasticity paradigms.
Highlights
Patterned neural activity and early sensory experience profoundly impact the development of organized circuit connectivity and can dramatically modify receptive field properties in the developing nervous system (Katz and Shatz, 1996; Holtmaat and Svoboda, 2009)
One of three standard induction protocols was applied: (1) for timing-dependent long-term potentiation (t-LTP), retinal stimulation was timed to evoke an EPSP 5–10 ms prior to the induction of an action potential in the tectal neuron (Figure 1C), (2) for timing-dependent long-term depression (t-LTD) the EPSP was timed to arrive 5–10 ms after the action potential (Figure 1D), and (3) a negative control protocol in which the interval between the action potential and the EPSP is outside the window to induce synaptic plasticity (+100 ms interval, Figure 1E)
Our study confirmed previous reports that repeated pairing of pre- and postsynaptic neuronal firing using a 5–10 ms EPSP-tospike interval is highly effective at driving retinotectal t-LTP and t-LTD in the developing Xenopus visual system
Summary
Patterned neural activity and early sensory experience profoundly impact the development of organized circuit connectivity and can dramatically modify receptive field properties in the developing nervous system (Katz and Shatz, 1996; Holtmaat and Svoboda, 2009). Computational models of activity-dependent map formation have traditionally employed a learning rule in which synapses between two neurons are strengthened in proportion to the degree of correlation in their firing (Abbott and Nelson, 2000). Such learning rules are sometimes referred to as “Hebbian”, in recognition of the Canadian psychologist Donald O. While many Hebbian models simplify this concept to reflect correlation in the firing rates of two cells, Hebb’s original formulation considered temporal causality
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