Neural changes in the primate brain correlated with the evolution of complex motor skills.

Y Yamazaki,K Hikishima,M Saiki,R N Lemon,M Inada,A Iriki,H Okano,E Sasaki,C J Price

doi:10.1038/srep31084

Abstract

Complex motor skills of eventual benefit can be learned after considerable trial and error. What do structural brain changes that accompany such effortful long-term learning tell us about the mechanisms for developing innovative behavior? Using MRI, we monitored brain structure before, during and after four marmosets learnt to use a rake, over a long period of 10–13 months. Throughout learning, improvements in dexterity and visuo-motor co-ordination correlated with increased volume in the lateral extrastriate cortex. During late learning, when the most complex behavior was maintained by sustained motivation to acquire the skill, the volume of the nucleus accumbens increased. These findings reflect the motivational state required to learn, and show accelerated function in higher visual cortex that is consistent with neurocognitive divergence across a spectrum of primate species.

Highlights

We identified three prominent areas of gray matter volume increase that correlated with higher performance scores or the rake distance moved (p < 0.05 after correction for multiple comparisons across the whole brain at the voxel level (familywise error (FWE) corrected): (i) the lateral extrastriate cortex (V2/V3), which are likely to reflect increased visuomotor control abilities in earlier stages; (ii) nucleus accumbens (Acb), which are likely to reflect strengthened reinforcing effects of effortful tool use in late learning stages; and (iii) the superior colliculus (SC), which are likely to reflect increased visual spatial attention to the food item and the tool
Intensive behavioral training has been reported to change brain volume in areas involved in the trained task[6]
The association of Acb with reward is consistent with previous studies that reported activation in Acb when the effort to get a reward increased[12], and when subjects learnt to perform a task skillfully[13]

Summary

Introduction

We identified three prominent areas of gray matter volume increase that correlated with higher performance scores or the rake distance moved (p < 0.05 after correction for multiple comparisons across the whole brain at the voxel level (familywise error (FWE) corrected): (i) the lateral extrastriate cortex (V2/V3), which are likely to reflect increased visuomotor control abilities in earlier stages; (ii) nucleus accumbens (Acb), which are likely to reflect strengthened reinforcing effects of effortful tool use in late learning stages; and (iii) the superior colliculus (SC), which are likely to reflect increased visual spatial attention to the food item and the tool. The location, time course and statistics related to Acb volume changes (i.e. change in the number of voxels identified as Acb region) in the later phase of learning are detailed in Fig. 2a,b, together with the coronal images corresponding to the same coordinates in the stereotaxic brain atlas[7].

Results

Conclusion