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The Journal of Neuroscience, September 28, 2005, 25(39):8854-8866; doi:10.1523/JNEUROSCI.1311-05.2005

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Behavioral/Systems/Cognitive
Quantitative Investigation of Connections of the Prefrontal Cortex in the Human and Macaque using Probabilistic Diffusion Tractography

Paula L. Croxson,^1,3 Heidi Johansen-Berg,¹ Timothy E. J. Behrens,¹ Matthew D. Robson,² Mark A. Pinsk,^4,5 Charles G. Gross,⁵ Wolfgang Richter,^4,6 Marlene C. Richter,⁴ Sabine Kastner,^4,5 and Matthew F. S. Rushworth^1,3

¹Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology and ²University of Oxford Centre for Clinical Magnetic Resonance Research, University of Oxford, John Radcliffe Hospital, Headington, Oxford OX3 9DU, United Kingdom, ³Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom, and ⁴Centre for the Study of Mind, Brain, and Behavior and Departments of ⁵Psychology and ⁶Chemistry, Princeton University, Princeton, New Jersey 08544

The functions of prefrontal cortex (PFC) areas are constrained by their anatomical connections. There is little quantitative information about human PFC connections, and, instead, our knowledge of primate PFC connections is derived from tracing studies in macaques. The connections of subcortical areas, in which white matter penetration and hence diffusion anisotropy are greatest, can be studied with diffusion-weighted imaging (DWI) tractography. We therefore used DWI tractography in four macaque and 10 human hemispheres to compare the connections of PFC regions with nine subcortical regions, including several fascicles and several subcortical nuclei. A distinct connection pattern was identified for each PFC and each subcortical region. Because some of the fascicles contained connections with posterior cortical areas, it was also possible to draw inferences about PFC connection patterns with posterior cortical areas. Notably, it was possible to identify similar circuits centered on comparable PFC regions in both species; PFC regions probably engage in similar patterns of regionally specific functional interaction with other brain areas in both species. In the case of one area traditionally assigned to the human PFC, the pars opercularis, the distribution of connections was not reminiscent of any macaque PFC region but, instead, resembled the pattern for macaque ventral premotor area. Some limitations to the DWI approach were apparent; the high diffusion anisotropy in the corpus callosum made it difficult to compare connection probability values in the adjacent cingulate region.

Key words: diffusion-weighted imaging; prefrontal cortex; projections; anatomy; subcortical; macaque MRI

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Received April 5, 2005; revised July 4, 2005; accepted August 14, 2005.

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