A history of spike-timing-dependent plasticity.

Henry Markram

doi:10.3389/fnsyn.2011.00004

Abstract

How learning and memory is achieved in the brain is a central question in neuroscience. Key to today’s research into information storage in the brain is the concept of synaptic plasticity, a notion that has been heavily influenced by Hebb's (1949) postulate. Hebb conjectured that repeatedly and persistently co-active cells should increase connective strength among populations of interconnected neurons as a means of storing a memory trace, also known as an engram. Hebb certainly was not the first to make such a conjecture, as we show in this history. Nevertheless, literally thousands of studies into the classical frequency-dependent paradigm of cellular learning rules were directly inspired by the Hebbian postulate. But in more recent years, a novel concept in cellular learning has emerged, where temporal order instead of frequency is emphasized. This new learning paradigm – known as spike-timing-dependent plasticity (STDP) – has rapidly gained tremendous interest, perhaps because of its combination of elegant simplicity, biological plausibility, and computational power. But what are the roots of today’s STDP concept? Here, we discuss several centuries of diverse thinking, beginning with philosophers such as Aristotle, Locke, and Ribot, traversing, e.g., Lugaro’s plasticità and Rosenblatt’s perceptron, and culminating with the discovery of STDP. We highlight interactions between theoretical and experimental fields, showing how discoveries sometimes occurred in parallel, seemingly without much knowledge of the other field, and sometimes via concrete back-and-forth communication. We point out where the future directions may lie, which includes interneuron STDP, the functional impact of STDP, its mechanisms and its neuromodulatory regulation, and the linking of STDP to the developmental formation and continuous plasticity of neuronal networks.

Highlights

Reviewed by: Kei Cho, University of Bristol, UK Takeshi Sakaba, Max Planck Institute for Biophysical Chemistry, Germany Yves Frégnac, CNRS UNIC, France Larry Abbott, Columbia University, USA
This mode of thinking is so human that concluding that B is caused by A in this scenario may make others accuse us of the logical fallacy of false cause, known as post hoc ergo propter hoc. This way of establishing causal and acausal relationships between events in the outside world seems to be key to how individual synaptic connections in the brain operate: typically, synapses are increased in strength if presynaptic spikes repeatedly occur before postsynaptic spikes within a few tens of milliseconds or less, whereas the opposite temporal order elicits synaptic weakening, a concept known as spike-timing-dependent plasticity (STDP; Figures 1A,B)
This study revealed long-term potentiation (LTP) for causal pre-beforepostsynaptics pike timings with 10 ms temporal displacement, while long-term depression (LTD) was elicited by acausal pre-after-postsynaptic spike timings, even though both conditions were elicited at the same frequency

Summary

SYNAPTIC NEUROSCIENCE

This mode of thinking is so human that concluding that B is caused by A in this scenario may make others accuse us of the logical fallacy of false cause, known as post hoc ergo propter hoc Even so, this way of establishing causal and acausal relationships between events in the outside world seems to be key to how individual synaptic connections in the brain operate: typically, synapses are increased in strength if presynaptic spikes repeatedly occur before postsynaptic spikes within a few tens of milliseconds or less, whereas the opposite temporal order elicits synaptic weakening, a concept known as spike-timing-dependent plasticity (STDP; Figures 1A,B). Philosophers have long argued as to whether we primarily are a product of nature or of nurture

History of STDP

CONCLUSIONS AND FUTURE DIRECTIONS

Key concepts