Plasticity of cardiorespiratory neural processing: classification and computational functions

Abstract

Neural plasticity, or malleability of neuronal structure and function, is an important attribute of the mammalian forebrain and is generally thought to be a kernel of biological intelligence. In this review, we examine some reported manifestations of neural plasticity in the cardiorespiratory system and classify them into four functional categories, integral; differential; memory; and statistical-type plasticity. At the cellular and systems level the myriad forms of cardiorespiratory plasticity display emergent and self-organization properties, use- and disuse-dependent and pairing-specific properties, short-term and long-term potentiation or depression, as well as redundancy in series or parallel structures, convergent pathways or backup and fail–safe surrogate pathways. At the behavioral level, the cardiorespiratory system demonstrates the capability of associative and nonassociative learning, classical and operant conditioning as well as short-term and long-term memory. The remarkable similarity and consistency of the various types of plasticity exhibited at all levels of organization suggest that neural plasticity is integral to cardiorespiratory control and may subserve important physiological functions.

Introduction

Classical models of cardiorespiratory control are predicated on the Sherrington view of sensory-motor reflex (Sherrington, 1906) in which afferent and efferent pathways are linked by anatomically distinct neural circuitry in the brain. This simple model adequately describes many stimulus-response behaviors including baroreflex, chemoreflex and Hering–Breuer reflex. Recent evidence, however, suggested that these stimulus-response relationships are not static but may exhibit stimulus-dependent adaptive changes over several time scales. The remarkable adaptability of cardiorespiratory responses implies that the corresponding reflex loops are not hardwired. Rather, they may undergo considerable plasticity in their structure and function, namely, adaptive modification or up/down regulation of synaptic transmission, neuronal connectivity or neuronal behavior over time and space. Mechanisms of such plasticity in the stimulus-response relationships may be multifarious and may occur at multiple sites from the afferent branch to efferent branch of each reflex loop. In this review, we examine and categorize various forms of plasticity in the cardiorespiratory system that develops immediately or shortly after afferent activation or deactivation. Emphasis is placed on the possible computational functions of such plasticity in cardiorespiratory control as well as their underlying mechanisms at the cellular and behavioral levels. Models and terminology deriving broadly from cellular, behavioral, and computational neuroscience literature are introduced for purpose of comparison and standardization of usage across different fields.

Specifically, we present direct and indirect evidence for four major classes of neural plasticity in cardiorespiratory afferent and efferent signal processing, integral; differential; statistical; and memory-type plasticity. The first three classes are phasic (memoryless) or short-term plasticity while the last one represents long-term plasticity. The various forms of plasticity together afford all basic mathematical operations for solving integral–differential and statistical equations and long-term memory storage, making the cardiorespiratory control system the equivalent of a pulse-coded analog computational device. In view of the similar and interdependent organization of the cardiovascular and respiratory systems it is not surprising that they share similar forms of plasticity, but differences also exist. Comparison of the plasticity exhibited in these systems may shed new light on the control mechanisms of both of them. Although these computational models pertain mainly to cardiorespiratory regulation, they are generally applicable to other types of sensory-motor reflexes — many of which exhibit similar forms of plasticity.