Abstract

In order to record the stream of autobiographical information that defines our unique personal history, our brains must form durable memories from single brief exposures to the patterned stimuli that impinge on them continuously throughout life. However, little is known about the computational strategies or neural mechanisms that underlie the brain's ability to perform this type of "online" learning. Based on increasing evidence that dendrites act as both signaling and learning units in the brain, we developed an analytical model that relates online recognition memory capacity to roughly a dozen dendritic, network, pattern, and task-related parameters. We used the model to determine what dendrite size maximizes storage capacity under varying assumptions about pattern density and noise level. We show that over a several-fold range of both of these parameters, and over multiple orders-of-magnitude of memory size, capacity is maximized when dendrites contain a few hundred synapses—roughly the natural number found in memory-related areas of the brain. Thus, in comparison to entire neurons, dendrites increase storage capacity by providing a larger number of better-sized learning units. Our model provides the first normative theory that explains how dendrites increase the brain’s capacity for online learning; predicts which combinations of parameter settings we should expect to find in the brain under normal operating conditions; leads to novel interpretations of an array of existing experimental results; and provides a tool for understanding which changes associated with neurological disorders, aging, or stress are most likely to produce memory deficits—knowledge that could eventually help in the design of improved clinical treatments for memory loss.

Highlights

  • To function well in a complex world, our brains must somehow stream our everyday experiences into memory as they occur in real time

  • Our mathematical model may prove useful in future efforts to understand how disruptions to dendritic structure and function lead to reduced memory capacity in aging and disease

  • A number of quantitative models have been proposed for palimpsest-style online memories, and have addressed a variety of different issues, including: how memory capacity scales with network size, how metaplastic learning rules can increase memory capacity, and the tradeoff between initial trace strength and memory lifetimes [1,2,3,4,5,6,7,8]

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Summary

Introduction

To function well in a complex world, our brains must somehow stream our everyday experiences into memory as they occur in real time. An “online” memory of this kind, once termed a “Palimpsest” [1], must be capable of forming durable memory traces from a single brief exposure to each incoming pattern, while preserving previously stored memories as long and faithfully as possible (Fig 1) This combined need for rapid imprinting and large capacity requires that the memory system carefully manage both its learning and forgetting processes, but we currently know little about how these processes are implemented and coordinated in the brain. This simplification is notable, given the substantial evidence from both modeling and experimental studies that dendritic trees are powerful, functionally compartmentalized information processors that can augment the computing capabilities of individual neurons in numerous ways [7,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59]

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