Eligibility Traces and Plasticity on Behavioral Time Scales: Experimental Support of NeoHebbian Three-Factor Learning Rules

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Journal:: “Frontiers in Neural Circuits” About:: Read:: - [ ] Gerstner et al. (2018) - Eligibility Traces and Plasticity on Behavioral Time Scales: Experimental Support of NeoHebbian Three-Factor Learning Rules ➕2025-11-04 !!2 rd citation todoist Print::  ❌ Zotero Link:: Zotero Files:: attachment Reading Note:: Web Rip:: url:: https://www.frontiersin.org/article/10.3389/fncir.2018.00053

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Abstract

Most elementary behaviors such as moving the arm to grasp an object or walking into the next room to explore a museum evolve on the time scale of seconds; in contrast, neuronal action potentials occur on the time scale of a few milliseconds. Learning rules of the brain must therefore bridge the gap between these two different time scales. Modern theories of synaptic plasticity have postulated that the co-activation of preand postsynaptic neurons sets a flag at the synapse, called an eligibility trace, that leads to a weight change only if an additional factor is present while the flag is set. This third factor, signaling reward, punishment, surprise, or novelty, could be implemented by the phasic activity of neuromodulators or specific neuronal inputs signaling special events. While the theoretical framework has been developed over the last decades, experimental evidence in support of eligibility traces on the time scale of seconds has been collected only during the last few years. Here we review, in the context of three-factor rules of synaptic plasticity, four key experiments that support the role of synaptic eligibility traces in combination with a third factor as a biological implementation of neoHebbian three-factor learning rules.

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Fig 1

FIGURE 1 | (A) Two Hebbian protocols and one three-factor learning protocol. (i) Hebbian STDP protocol with presynaptic spikes (presynaptic factor) followed by a burst of postsynaptic spikes (postsynaptic factor). Synapses in the stimulated pathway (green) will typically show LTP while an unstimulated synapse (red) will not change its weight (Markram et al., 1997). (ii) Hebbian voltage pairing protocol of presynaptic spikes (presynaptic factor) with a depolarization of the postsynaptic neuron (postsynaptic factor). Depending on the amount of depolarization the stimulated pathway (green) will show LTP or LTD while an unstimulated synapse (red) does not change its weight (Artola and Singer, 1993; Ngezahayo et al., 2000). (iii) Results of a Hebbian induction protocol are influenced by a third factor (blue) even if it is given after a delay d. The third factor could be a neuromodulator such as dopamine, acetylcholine, noreprinephrine, or serotonin (Pawlak et al., 2010; Yagishita et al., 2014; Brzosko et al., 2015, 2017; He et al., 2015; Bittner et al., 2017). (B) Specificity of three-factor learning rules. (i) Presynaptic input spikes (green) arrive at two different neurons, but only one of these also shows postsynaptic activity (orange spikes). (ii) A synaptic flag is set only at the synapse with a Hebbian co-activation of preand postsynaptic factors; the synapse become then eligible to interact with the third factor (blue). Spontaneous spikes of other neurons do not interfere. (iii) The interaction of the synaptic flag with the third factor leads to a strengthening of the synapse (green). Page 4

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Fig 1