A history of spike-timing-dependent plasticity

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.

Keywords: bidirectional plasticity; history; learning; long term depression; long term plasticity; memory; spike-timing-dependent plasticity; synaptic plasticity.

Figure 1

Defining Spike-Timing-Dependent Plasticity (A) A presynaptic cell connected to a postsynaptic cell repeatedly spiking just before the latter is in part causing it to spike, while the opposite order is acausal. (B) In typical STDP, causal activity results in long-term potentiation (LTP), while acausal activity elicits long-term depression (LTD; Markram et al., ; Bi and Poo, ; Zhang et al., 1998). At some cortical synapses, the temporal window for LTD (dashed gray line) is extended (Feldman, ; Sjöström et al., 2001). These temporal windows are often also activity dependent, with LTP being absent at low-frequency (gray continuous line, Markram et al., ; Sjöström et al., 2001), and postsynaptic bursting relaxing the LTD timing requirements to hundreds of milliseconds (Debanne et al., ; Sjöström et al., 2003).

Figure 2

William James Source: Houghton Library, Harvard University, Call number pfMS Am 1092 (1185) #83, with permission.

Figure 3

Santiago Ramón y Cajal Source: Wikimedia Commons, public domain.

Figure 4

Donald Hebb.

Figure 5

An illustration of the Hebbian postulate and a small assembly of cells. Here, presynaptic cell a, along with afferents c and d, repeatedly and persistently drive the postsynaptic cell b, thus leading to a long-term increase in the connective strength between cells a and b (reprinted with permission from Hebb, 1972).

Figure 6

Tim Bliss, Per Andersen, Terje Lømo.

Figure 7

Sir Bernard Katz.