Spike timing dependent plasticity: a consequence of more fundamental learning rules

Abstract

Spike timing dependent plasticity (STDP) is a phenomenon in which the precise timing of spikes affects the sign and magnitude of changes in synaptic strength. STDP is often interpreted as the comprehensive learning rule for a synapse – the “first law” of synaptic plasticity. This interpretation is made explicit in theoretical models in which the total plasticity produced by complex spike patterns results from a superposition of the effects of all spike pairs. Although such models are appealing for their simplicity, they can fail dramatically. For example, the measured single-spike learning rule between hippocampal CA3 and CA1 pyramidal neurons does not predict the existence of long-term potentiation one of the best-known forms of synaptic plasticity. Layers of complexity have been added to the basic STDP model to repair predictive failures, but they have been outstripped by experimental data. We propose an alternate first law: neural activity triggers changes in key biochemical intermediates, which act as a more direct trigger of plasticity mechanisms. One particularly successful model uses intracellular calcium as the intermediate and can account for many observed properties of bidirectional plasticity. In this formulation, STDP is not itself the basis for explaining other forms of plasticity, but is instead a consequence of changes in the biochemical intermediate, calcium. Eventually a mechanism-based framework for learning rules should include other messengers, discrete change at individual synapses, spread of plasticity among neighboring synapses, and priming of hidden processes that change a synapse's susceptibility to future change. Mechanism-based models provide a rich framework for the computational representation of synaptic plasticity.

Time scales of memory, learning, and plasticity

“…The plasticity processes as such are related to LTP and LTD as discussed previously. However, the generality of STDP is heavily debated (Lisman andSpruston 2005, 2010;Shouval et al 2010). Experiments show that the temporal order is only important in a small regime of presynaptic activation (Sjöström et al 2001) and, furthermore, that synaptic modifications seem to be independent of the spiking of the postsynaptic cell (Golding et al 2002).…”

Numerical modelling of plasticity induced by transcranial magnetic stimulation

“…While the validity of a simple formulation of STDP is still a matter of some debate [43,27] it leads to a straightforward modelling scheme. An alternative approach has been taken by Fung and Robinson [12] in which calcium dependent plasticity has been modelled.…”

Calcium control of triphasic hippocampal STDP

“…(f) Overall synaptic weight change generated in our model by 100 pre-synaptic inputs delivered at 2Hz while the post-synaptic membrane voltage is held fixed at various levels of depolarisation, with the same parameter values as (b) One issue with the interpretation of empirical plasticity data obtained using tetanic stimulation protocols is the fact that post-synaptic activity is rarely recorded, but has a significant impact on the magnitude of NMDAr-[Ca 2+ ] generated. In fact, experimental evidence suggests that post-synaptic activity is a necessary requirement for any form of synaptic plasticity, although contradictory reports do exist [32,58,59]. Wittenberg and Wang [29] provide unique data regarding the induction of LTD by a single LFS protocol (900 pulses at 3.3Hz), in that the response of the post-synaptic neuron was recorded throughout pre-synaptic stimulation -as 200 action potentials which each followed input volleys with a latency of 6.2 ± 4ms.…”

“…However, more recent examinations using acute hippocampal slices have been unable to induce bidirectional plasticity with pairs of single preand post-synaptic action potentials under standard recording conditions [ Figure 1b; 28-30, 33, 34]. These results suggest a more complex picture, where synaptic plasticity is dependent not just on relative spike timing, but also on the frequency, duration and nature of spike pairings -with a triphasic STDP curve obtained at CA3-CA1 synapses only when pairings are delivered at approximately theta frequency (>5Hz) and involve multiple post-synaptic spikes [20,29,32; Figure 1c]. Similar results have been obtained at excitatory connections between cortical pyramidal neurons [35].…”

“…In more recent years, it has also been established that temporally correlated pairs or triplets of pre-and post-synaptic action potentials delivered at low frequencies can induce bidirectional spike-timing dependent plasticity (STDP) depending, among other parameters, on their exact temporal offset over a range of ~100ms [26][27][28][29][30]. STDP has been examined in a variety of cortical regions and species, and its discovery has both accompanied and accelerated a move in computational neuroscience from rate to temporally coded models of cognitive processing [31,32]. …”