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Neural Computation

November 2018, Vol. 30, No. 11, Pages 3037-3071
(doi: 10.1162/neco_a_01128)
© 2018 Massachusetts Institute of Technology
Circuit Polarity Effect of Cortical Connectivity, Activity, and Memory
Article PDF (1.24 MB)
Experimental constraints have traditionally implied separate studies of different cortical functions, such as memory and sensory-motor control. Yet certain cortical modalities, while repeatedly observed and reported, have not been clearly identified with one cortical function or another. Specifically, while neuronal membrane and synapse polarities with respect to a certain potential value have been attracting considerable interest in recent years, the purposes of such polarities have largely remained a subject for speculation and debate. Formally identifying these polarities as on-off neuronal polarity gates, we analytically show that cortical circuit structure, behavior, and memory are all governed by the combined potent effect of these gates, which we collectively term circuit polarity. Employing widely accepted and biologically validated firing rate and plasticity paradigms, we show that circuit polarity is mathematically embedded in the corresponding models. Moreover, we show that the firing rate dynamics implied by these models are driven by ongoing circuit polarity gating dynamics. Furthermore, circuit polarity is shown to segregate cortical circuits into internally synchronous, externally asynchronous subcircuits, defining their firing rate modes in accordance with different cortical tasks. In contrast to the Hebbian paradigm, which is shown to be susceptible to mutual neuronal interference in the face of asynchrony, circuit polarity is shown to block such interference. Noting convergence of synaptic weights, we show that circuit polarity holds the key to cortical memory, having a segregated capacity linear in the number of neurons. While memory concealment is implied by complete neuronal silencing, memory is restored by reactivating the original circuit polarity. Finally, we show that incomplete deterioration or restoration of circuit polarity results in memory modification, which may be associated with partial or false recall, or novel innovation.