The Scale of Functional Specialization within Human Prefrontal Cortex

At what scale is it possible to observe consistent functional specialization within human prefrontal cortex (PFC), reproducible from one individual to the next? Some studies suggest gross functional divisions between large regions of PFC, but it is not known whether PFC exhibits specialization at the fine-grained scale known to differentiate posterior cortical functions. We used fMRI to confirm a three-way segregation of function between three regions of medial anterior PFC, each centered on coordinates within 15 mm of the other two. Naive participants performed three tasks based on earlier studies, and we investigated activity at regions defined by previous results. In each task, signal was significantly greater at the predicted region than the other two, just millimeters away. These results indicate reproducible functional specialization within PFC, at a much finer scale than previously demonstrated. Furthermore, these findings suggest that divergent results from previous studies may reflect the recruitment of functionally distinct regions and that “reverse inference” should be undertaken with caution.

[1]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[2]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[3]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[5]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[6]  C. Frith,et al.  Distinct regions of medial rostral prefrontal cortex supporting social and nonsocial functions. , 2007, Social cognitive and affective neuroscience.

[7]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[8]  Paul C. Fletcher,et al.  Separable Forms of Reality Monitoring Supported by Anterior Prefrontal Cortex , 2008, Journal of Cognitive Neuroscience.

[9]  Jordan Grafman,et al.  Event frequency modulates the processing of daily life activities in human medial prefrontal cortex. , 2007, Cerebral cortex.

[10]  R. Henson What can Functional Neuroimaging Tell the Experimental Psychologist? , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[11]  M. Schölvinck,et al.  Differential components of prospective memory? Evidence from fMRI , 2006, Neuropsychologia.

[12]  Richard Henson,et al.  Forward inference using functional neuroimaging: dissociations versus associations , 2006, Trends in Cognitive Sciences.

[13]  Paul C. Fletcher,et al.  Anterior prefrontal cortex and the recollection of contextual information , 2005, Neuropsychologia.

[14]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[15]  Iroise Dumontheil,et al.  The gateway hypothesis of rostral prefrontal cortex (area 10) function , 2007, Trends in Cognitive Sciences.

[16]  R. Benoit,et al.  Mesulam's frontal lobe mystery re-examined. , 2009, Restorative neurology and neuroscience.

[17]  Stephen Lawrie,et al.  Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis , 2006, Journal of Cognitive Neuroscience.

[18]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[19]  R. Poldrack Can cognitive processes be inferred from neuroimaging data? , 2006, Trends in Cognitive Sciences.

[20]  P. Goldman-Rakic,et al.  Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys , 1981, The Journal of comparative neurology.

[21]  U. Frith,et al.  The impact of extensive medial frontal lobe damage on 'Theory of Mind' and cognition. , 2004, Brain : a journal of neurology.

[22]  E. Koechlin,et al.  Anterior Prefrontal Function and the Limits of Human Decision-Making , 2007, Science.

[23]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[24]  C. Frith,et al.  Involvement of rostral prefrontal cortex in selection between stimulus‐oriented and stimulus‐independent thought , 2005, The European journal of neuroscience.