Coherent noise enables probabilistic sequence replay in spiking neuronal networks

Author summaryHumans and other animals often benefit from exploring multiple alternative solutions to a given problem, rather than adhering to a single, global optimum. Such explorative behavior is frequently attributed to noise in the neuronal dynamics. Supplying each neuron or synapse in a neuronal circuit with noise, however, does not necessarily lead to explorative dynamics. If decisions are triggered by the compound activity of ensembles of neurons or synapses, noise averages out, unless it is correlated within these ensembles. As an analogy, consider a particle in a still fluid: despite the constant bombardment by surrounding molecules, a large particle will hardly undergo any Brownian motion, because the momenta of the impinging molecules largely cancel each other. Only if the molecules move in a coherent manner, such as in a turbulent fluid, they can have a substantial influence on the particle's motion. This modeling study exploits this effect to equip a neuronal sequence-processing circuit with explorative behavior by introducing configurable, locally coherent noise. It contributes to an understanding of the neuronal mechanisms underlying different decision strategies in the face of ambiguity, and highlights the role of coherent network activity such as traveling waves during sequential memory recall. Animals rely on different decision strategies when faced with ambiguous or uncertain cues. Depending on the context, decisions may be biased towards events that were most frequently experienced in the past, or be more explorative. A particular type of decision making central to cognition is sequential memory recall in response to ambiguous cues. A previously developed spiking neuronal network implementation of sequence prediction and recall learns complex, high-order sequences in an unsupervised manner by local, biologically inspired plasticity rules. In response to an ambiguous cue, the model deterministically recalls the sequence shown most frequently during training. Here, we present an extension of the model enabling a range of different decision strategies. In this model, explorative behavior is generated by supplying neurons with noise. As the model relies on population encoding, uncorrelated noise averages out, and the recall dynamics remain effectively deterministic. In the presence of locally correlated noise, the averaging effect is avoided without impairing the model performance, and without the need for large noise amplitudes. We investigate two forms of correlated noise occurring in nature: shared synaptic background inputs, and random locking of the stimulus to spatiotemporal oscillations in the network activity. Depending on the noise characteristics, the network adopts various recall strategies. This study thereby provides potential mechanisms explaining how the statistics of learned sequences affect decision making, and how decision strategies can be adjusted after learning.

Automated summary

Humans and other animals benefit from exploring multiple alternative solutions to problems, rather than relying on a single optimal solution. This explorative behavior is often attributed to noise in neuronal dynamics. However, equipping a neuronal circuit with noise does not necessarily lead to explorative dynamics unless the noise is correlated within ensembles. This modeling study introduces configurable, locally coherent noise to create explorative behavior in a neuronal sequence-processing circuit, contributing to understanding the neuronal mechanisms underlying decision strategies and sequential memory recall.