Spike-Time-Dependent Plasticity and Heterosynaptic Competition Organize Networks to Produce Long Scale-Free Sequences of Neural Activity

• Published in: Neuron (Cambridge, Mass.) Vol. 65; no. 4; pp. 563 - 576
• Main Authors: Fiete, Ila R., Senn, Walter, Wang, Claude Z.H., Hahnloser, Richard H.R.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 25.02.2010; Elsevier Limited
• Subjects: Action Potentials - physiology; Animals; Behavior; Brain; Competition; Electrophysiology; Finches; High Vocal Center - physiology; Learning - physiology; Membrane Potentials - physiology; Models, Neurological; Nerve Net - physiology; Neural Conduction - physiology; Neuronal Plasticity - physiology; Neurons; Neurons - physiology; SIGNALING; Synapses - physiology; SYSBIO; SYSNEURO; SYSNEURO; SYSBIO; SIGNALING
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2010.02.003

Sequential neural activity patterns are as ubiquitous as the outputs they drive, which include motor gestures and sequential cognitive processes. Neural sequences are long, compared to the activation durations of participating neurons, and sequence coding is sparse. Numerous studies demonstrate that spike-time-dependent plasticity (STDP), the primary known mechanism for temporal order learning in neurons, cannot organize networks to generate long sequences, raising the question of how such networks are formed. We show that heterosynaptic competition within single neurons, when combined with STDP, organizes networks to generate long unary activity sequences even without sequential training inputs. The network produces a diversity of sequences with a power law length distribution and exponent −1, independent of cellular time constants. We show evidence for a similar distribution of sequence lengths in the recorded premotor song activity of songbirds. These results suggest that neural sequences may be shaped by synaptic constraints and network circuitry rather than cellular time constants. ► STDP and heterosynaptic competition can organize random networks to generate sequences ► The neural activity sequences are models of modular and unary premotor codes ► Sequences of length L occur with frequency ∼1/L, consistent with zebra finch song data ► Sequence formation may be a network processes, not requiring slow cellular processes