Abstract

The aging brain shows a progressive loss of neuropil, which is accompanied by subtle changes in neuronal plasticity, sensory learning and memory. Neurophysiologically, aging attenuates evoked responses—including the mismatch negativity (MMN). This is accompanied by a shift in cortical responsivity from sensory (posterior) regions to executive (anterior) regions, which has been interpreted as a compensatory response for cognitive decline. Theoretical neurobiology offers a simpler explanation for all of these effects—from a Bayesian perspective, as the brain is progressively optimized to model its world, its complexity will decrease. A corollary of this complexity reduction is an attenuation of Bayesian updating or sensory learning. Here we confirmed this hypothesis using magnetoencephalographic recordings of the mismatch negativity elicited in a large cohort of human subjects, in their third to ninth decade. Employing dynamic causal modeling to assay the synaptic mechanisms underlying these non-invasive recordings, we found a selective age-related attenuation of synaptic connectivity changes that underpin rapid sensory learning. In contrast, baseline synaptic connectivity strengths were consistently strong over the decades. Our findings suggest that the lifetime accrual of sensory experience optimizes functional brain architectures to enable efficient and generalizable predictions of the world.

Highlights

  • Aging is generally thought to be accompanied by reduced neuronal plasticity and a loss of neuronal processes that accounts for a loss of grey matter, which progresses gently with age [1,2,3]

  • We examine the physiological basis of attenuated mismatch responses using dynamic causal modeling in a large cohort of human subjects

  • We address the corollary of model complexity minimization; namely, less reliance on Bayesian updating through sensory learning and underlying neuronal plasticity

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Summary

Introduction

Aging is generally thought to be accompanied by reduced neuronal plasticity and a loss of neuronal processes that accounts for a loss of grey matter, which progresses gently with age [1,2,3]. Many concomitants of physiological aging have been studied. Studies of the mismatch negativity (MMN) speak to a decline in sensory learning or memory [4,5]. Elderly subjects show a significant reduction in superior temporal gyrus responses, which has been interpreted as ‘‘an aging-related decline in auditory sensory memory and automatic change detection’’ [6]. We examine the physiological basis of attenuated mismatch responses using dynamic causal modeling in a large cohort of human subjects. We motivate the present study using an alternative – and slightly more optimistic – model of normal aging

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