Gray and white matter changes associated with tool-use learning in macaque monkeys

Abstract

We used noninvasive MRI and voxel-based morphometry (VBM) to detect changes in brain structure in three adult Japanese macaques trained to use a rake to retrieve food rewards. Monkeys, who were naive to any previous tool use, were scanned repeatedly in a 4-T scanner over 6 weeks, comprising 2 weeks of habituation followed by 2 weeks of intensive daily training and a 2-week posttraining period. VBM analysis revealed significant increases in gray matter with rake performance across the three monkeys. The effects were most significant (P < 0.05 corrected for multiple comparisons across the whole brain) in the right superior temporal sulcus, right second somatosensory area, and right intraparietal sulcus, with less significant effects (P < 0.001 uncorrected) in these same regions of the left hemisphere. Bilateral increases were also observed in the white matter of the cerebellar hemisphere in lobule 5. In two of the monkeys who exhibited rapid learning of the rake task, gray matter volume in peak voxels increased by up to 17% during the intensive training period; the earliest changes were seen after 1 week of intensive training, and they generally peaked when performance on the task plateaued. In the third monkey, who was slower to learn the task, peak voxels showed no systematic changes. Thus, VBM can detect significant brain changes in individual trained monkeys exposed to tool-use training for the first time. This approach could open up a means of investigating the underlying neurobiology of motor learning and other higher brain functions in individual animals.intraparietal sulcus ͉ second somatosensory area ͉ superior temporal sulcus ͉ voxel-based morphometry T he brain exhibits use-dependent structural flexibility, which is far greater than realized previously and which is detectable even at a macroscopic level and in adulthood. Structural MRI studies of the human brain have demonstrated differences in the hippocampus of experienced London taxi drivers (1), a relationship between musical proficiency and the volume of motor and auditory cortex (2), enlarged prefrontal and parietal areas in mathematicians (3), and increased inferior parietal gray matter density in adolescents with enriched vocabulary knowledge (4). There is also an extensive literature on the effect of experience-driven plasticity in animals (see refs. 5-7).In humans, rapid changes in gray matter after the acquisition of a new motor skill were demonstrated by Draganski et al. (8): after 3 months of learning to juggle, gray matter increases were observed in the extrastriate motion area and the posterior intraparietal sulcus. These changes were detected with voxel-based morphometry (VBM) after pooling data from a large group of human subjects. The neurobiological underpinnings of structural brain changes associated with the acquisition of new skills remain unknown and could involve a wide variety of different neuronal mechanisms, including angiogenesis and even neurogenesis (9). Ultimately, invasive experiments in an animal model will be needed to ...

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Individual and social learning processes involved in the acquisition and generalization of tool use in macaques

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MRI Techniques and New Animal Models for Imaging the Brain

“…Voxel-wise statistical tests are then performed on these tissue maps to identify group-wise differences or longitudinal changes based on the General Linear Model (GLM) (Ashburner & Friston 2000). For example, a longitudinal paradigm has revealed that training induces grey/white matter volume changes in macaques (Quallo et al 2009). VBM can also highlight phenotypic variations.…”