Modeling the Dynamic Interaction of Hebbian and Homeostatic Plasticity

• Published in: Neuron (Cambridge, Mass.) Vol. 84; no. 2; pp. 497 - 510
• Main Authors: Toyoizumi, Taro, Kaneko, Megumi, Stryker, Michael P., Miller, Kenneth D.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 22.10.2014; Elsevier Limited
• Subjects: Animals; Biomedical research; Charitable foundations; Dominance, Ocular - physiology; Experiments; Feedback; Homeostasis; Homeostasis - physiology; Laboratory animals; Male; Mice, Inbred C57BL; Models, Neurological; Neuronal Plasticity - physiology; Neurons - physiology; Noise; Ordinary differential equations; Random variables; Synapses - physiology; Time Factors
• ISSN: 0896-6273; 1097-4199; 1097-4199
• DOI: 10.1016/j.neuron.2014.09.036

Hebbian and homeostatic plasticity together refine neural circuitry, but their interactions are unclear. In most existing models, each form of plasticity directly modifies synaptic strength. Equilibrium is reached when the two are inducing equal and opposite changes. We show that such models cannot reproduce ocular dominance plasticity (ODP) because negative feedback from the slow homeostatic plasticity observed in ODP cannot stabilize the positive feedback of fast Hebbian plasticity. We propose a model in which synaptic strength is the product of a synapse-specific Hebbian factor and a postsynaptic-cell-specific homeostatic factor, with each factor separately arriving at a stable inactive state. This model captures ODP dynamics and has plausible biophysical substrates. We confirm model predictions experimentally that plasticity is inactive at stable states and that synaptic strength overshoots during recovery from visual deprivation. These results highlight the importance of multiple regulatory pathways for interactions of plasticity mechanisms operating over separate timescales. •Existing models cannot reproduce slow homeostatic plasticity under visual deprivation•The problem: slow homeostatic plasticity cannot stabilize Hebbian plasticity•Our solution: synaptic weights a product of separate homeostatic and Hebbian factors•New predictions confirmed: no ongoing plasticity; recovery induces weight overshoot How do Hebbian and homeostatic plasticity interact? Toyoizumi et al. show that existing models cannot explain ocular dominance plasticity. They propose instead that the two forms of plasticity control separate biochemical factors underlying synaptic strength. New experiments confirm model predictions.