Biological development of reading circuits

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Human neuroimaging is expanding our understanding of the biological processes that are essential for healthy brain function. Methods such as diffusion weighted imaging provide insights into white matter fascicles, growth and pruning of dendritic arbors and axons, and properties of glia. This review focuses on what we have learned from diffusion imaging about these processes and the development of reading circuitry in the human brain. Understanding reading circuitry development may suggest ways to improve how we teach children to read.

Highlights

► Cognitive skills, such as reading, depend on long-term development of axons and glia. ► Diffusion weighted MRI can assess tissue properties of specific reading circuits. ► Biological models of the reading circuitry can predict children's reading skills.

Introduction

A generation of cognitive neuroscientists has pursued the idea that the neurobiological principles of perception, learning and memory can be understood by analyzing synaptic properties in simple model organisms, or by measuring action potentials in small collections of neurons [1]. The emphasis on synapse and spiking is reflected in computational theories, which give a central role to synaptic efficacy [2, 3].

Human neuroimaging methods inform us about brain processes beyond synapses and spikes. Functional MRI (fMRI) measures integrative metabolic signals [4]; EEG/MEG methods measure extra synaptic mean field potentials [5, 6]. Diffusion weighted imaging and tractography measure the long-range axonal projections that carry signals between distant cortical regions [7]; quantitative MRI methods [8] can assess tissue properties of neurons and also the near by glia, whose function are significant throughout the lifespan [9••]. For example, glia have an essential role in cortical circuit formation [10, 11, 12], glial properties are shaped by experience during critical periods [13], and glia influence axonal transmission [14, 15]. Just like the synapse, the properties of tracts and tissue influence cognition and behavior [16, 17, 18, 19, 20••].

Given the expanded opportunity to measure such processes, what might be learned from these measurements? Some behaviors, such as psychological tests of performance during brief trials, may be best understood by measuring synaptic activity or spikes. But other important behaviors, such as learning to read, acquiring a second language, or learning to regulate emotions, take place over longer time periods and may depend on biological processes such as cell development, growth and pruning of dendritic arbors, the proliferation and activity of glia, axon myelination and pruning, and vascular development. Ultimately, neuroscientists and clinicians will need to account for the entire range of processes to understand circuit function in health and disease.

This review focuses on how one of the new neuroimaging modalities, diffusion weighted magnetic resonance imaging, informs us about reading circuitry in the human brain. The neurobiology of reading has been an active research area [21, 22, 23, 24, 25, 26] because many scientists would like to understand how the integration of signals across visual, auditory and language circuits implements this uniquely human cognitive process. Furthermore, there is a hope that understanding the reading circuits will lead us to develop ways to improve how we teach children to read. Here we provide a brief and opinionated discussion of recent findings centered on the information provided by diffusion-weighted imaging (DWI) about reading circuitry. We conclude by discussing how these findings might matter for society.

Section snippets

Background

Instrumentation and algorithms to measure white matter connections in the living human brain advanced dramatically in the1990s; diffusion-weighted MRI coupled with tractography algorithms provided spatially resolved measurements of specific white matter pathways in the living human brain [27, 28, 29, 30]. Perhaps Klingberg and colleagues [31] were the first to take advantage of the opportunity to relate white matter properties to cognition. The idea of the measurement still seems remarkable:

Reading circuitry

Diffusion weighted imaging measures suggest that several large fascicles beyond the early visual pathways are part of the reading circuitry. Specifically, diffusion measures consistently reveal associations between diffusion and reading skills in three major tracts: the posterior corpus callosum, the arcuate fasciculus and the inferior longitudinal fasciculus (Figure 1). These are large fascicles that contain axons between many different cortical regions, and they certainly carry information

Circuit and tissue development

At what age do the neurobiological differences between good and poor readers arise? The Klingberg et al. findings in adult were replicated in two independent samples of children [32, 33]. Hence, these differences are present at an early age and do not change substantially over the course of reading instruction. Earlier in this article we suggested that the diffusivity differences reported by Klingberg et al. might be explained by the relative size and position of the corona radiata, arcuate

Prediction and prevention of poor reading

There has been good progress developing simple behavioral measures to predict which children are at risk for a reading disability. Children in kindergarten and 1st grade who have difficulty naming letters and little ability to distinguish or blend individual sounds are likely to be poor readers in the 4th grade [61••]. We are less skilled at selecting interventions to help children who are poor readers at the end of first grade become average readers by the end of elementary school [62, 63].

Conclusions

Brain computations operate over a range of temporal and spatial scales. Understanding action potentials and synaptic efficacy is essential for understanding certain aspects of performance. Other forms of behavior, perhaps learning that takes place over the time scale of cognitive development, may depend on multiple biological processes including those that operate over time scales from hours to days to years. Cognitive neuroscientists can now measure and consider the influence of a wide range

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgments

We thank Franco Pestilli and Jon Winawer for comments. Supported by NIH R01-EY15000 (BAW) and NSF Graduate Research Fellowship (JDY).

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