The Brain Ages Optimally to Model Its Environment: Evidence from Sensory Learning over the Adult Lifespan

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.

Author Summary

While studies of aging are widely framed in terms of their demarcation of degenerative processes, the brain provides a unique opportunity to uncover the adaptive effects of getting older. Though intuitively reasonable, that life-experience and wisdom should reside somewhere in human cortex, these features have eluded neuroscientific explanation. The present study utilizes a “Bayesian Brain” framework to motivate an analysis of cortical circuit processing. From a Bayesian perspective, the brain represents a model of its environment and offers predictions about the world, while responding, through changing synaptic strengths to novel interactions and experiences. We hypothesized that these predictive and updating processes are modified as we age, representing an optimization of neuronal architecture. Using novel sensory stimuli we demonstrate that synaptic connections of older brains resist trial by trial learning to provide a robust model of their sensory environment. These older brains are capable of processing a wider range of sensory inputs – representing experienced generalists. We thus explain how, contrary to a singularly degenerative point-of-view, aging neurobiological effects may be understood, in sanguine terms, as adaptive and useful.