Understanding the long association pathways that convey cortical connections is a critical step in exploring the anatomic substrates of cognition in health and disease. Diffusion tensor imaging (DTI) is able to demonstrate fibre tracts non-invasively, but present approaches have been hampered by the inability to visualize fibres that have intersecting trajectories (crossing fibres), and by the lack of a detailed map of the origins, course and terminations of the white matter pathways. We therefore used diffusion spectrum imaging (DSI) that has the ability to resolve crossing fibres at the scale of single MRI voxels, and identified the long association tracts in the monkey brain. We then compared the results with available expositions of white matter pathways in the monkey using autoradiographic histological tract tracing. We identified 10 long association fibre bundles with DSI that match the observations in the isotope material: emanating from the parietal lobe, the superior longitudinal fasciculus subcomponents I, II and III; from the occipital-parietal region, the fronto-occipital fasciculus; from the temporal lobe, the middle longitudinal fasciculus and from rostral to caudal, the uncinate fasciculus, extreme capsule and arcuate fasciculus; from the occipital-temporal region, the inferior longitudinal fasciculus; and from the cingulate gyrus, the cingulum bundle. We suggest new interpretations of the putative functions of these fibre bundles based on the cortical areas that they link. These findings using DSI and validated with reference to autoradiographic tract tracing in the monkey represent a considerable advance in the understanding of the fibre pathways in the cerebral white matter. By replicating the major features of these tracts identified by histological techniques in monkey, we show that DSI has the potential to cast new light on the organization of the human brain in the normal state and in clinical disorders.