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 pre- and 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.
Highlights
Humans are able to learn novel behaviors such as pressing a button, swinging a tennis racket, or braking at a red traffic light; they are able to form memories of salient events, learn to distinguish flowers, and to establish a mental map when exploring a novel environment
spike-timing dependent plasticity (STDP) under the control of neuromodulators leads to the framework of three-factor learning rules (Xie and Seung, 2004; Legenstein et al, 2008; Vasilaki et al, 2009) where an eligibility trace represents the Hebbian idea of co-activation of pre- and postsynaptic neurons (Hebb, 1949) while modulation of plasticity by additional gating signals is represented generically by a “third factor” (Crow, 1968; Barto, 1985; Legenstein et al, 2008)
The framework is experimentally well-established in the context of synaptic consolidation where the duration of the flag (“synaptic tag”) extracted from slice experiments (Frey and Morris, 1997) is in the range of 1 h, consistent with fear conditioning experiments (Moncada and Viola, 2007). This time scale is significantly longer than what is needed for behavioral learning of elementary actions or for memorizing surprising events
Summary
Humans are able to learn novel behaviors such as pressing a button, swinging a tennis racket, or braking at a red traffic light; they are able to form memories of salient events, learn to distinguish flowers, and to establish a mental map when exploring a novel environment. STDP under the control of neuromodulators leads to the framework of three-factor learning rules (Xie and Seung, 2004; Legenstein et al, 2008; Vasilaki et al, 2009) where an eligibility trace represents the Hebbian idea of co-activation of pre- and postsynaptic neurons (Hebb, 1949) while modulation of plasticity by additional gating signals is represented generically by a “third factor” (Crow, 1968; Barto, 1985; Legenstein et al, 2008). Before we turn to three-factor rules, let us discuss conventional models of Hebbian learning
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