Broca’s region: linking human brain functional connectivity data and non-human primate tracing anatomy studies

Authors

  • Clare Kelly,

    1. The Phyllis Green and Randolph Cowen Institute for Pediatric Neuroscience, New York University Child Study Center, New York, NY 10016, USA
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    • C.K. and L.Q.U. contributed equally to this work.

  • Lucina Q. Uddin,

    1. Department of Psychiatry, Stanford University School of Medicine, Stanford, CA, USA
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    • C.K. and L.Q.U. contributed equally to this work.

  • Zarrar Shehzad,

    1. The Phyllis Green and Randolph Cowen Institute for Pediatric Neuroscience, New York University Child Study Center, New York, NY 10016, USA
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  • Daniel S. Margulies,

    1. Berlin School of Mind and Brain, Humboldt Universitat, Berlin, Germany
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  • F. Xavier Castellanos,

    1. The Phyllis Green and Randolph Cowen Institute for Pediatric Neuroscience, New York University Child Study Center, New York, NY 10016, USA
    2. The Nathan Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
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  • Michael P. Milham,

    1. The Phyllis Green and Randolph Cowen Institute for Pediatric Neuroscience, New York University Child Study Center, New York, NY 10016, USA
    2. The Nathan Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
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  • Michael Petrides

    1. Montreal Neurological Institute, McGill University, Montreal, QC H3A2B4, Canada
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Dr Michael P. Milham and Dr Michael Petrides, as above.
E-mails: michael.milham@nyumc.org and michael.petrides@mcgill.ca

Abstract

Brodmann areas 6, 44 and 45 in the ventrolateral frontal cortex of the left hemisphere of the human brain constitute the anterior language production zone. The anatomical connectivity of these areas with parietal and temporal cortical regions was recently examined in an autoradiographic tract-tracing study in the macaque monkey. Studies suggest strong correspondence between human resting state functional connectivity (RSFC) based on functional magnetic resonance imaging data and experimentally demonstrated anatomical connections in non-human primates. Accordingly, we hypothesized that areas 6, 44 and 45 of the human brain would exhibit patterns of RSFC consistent with patterns of anatomical connectivity observed in the macaque. In a primary analysis, we examined the RSFC associated with regions-of-interest placed in ventrolateral frontal areas 6, 44 and 45, on the basis of local sulcal and gyral anatomy. We validated the results of the primary hypothesis-driven analysis with a data-driven partitioning of ventrolateral frontal cortex into regions exhibiting distinct RSFC patterns, using a spectral clustering algorithm. The RSFC of ventrolateral frontal areas 6, 44 and 45 was consistent with patterns of anatomical connectivity shown in the macaque. We observed a striking dissociation between RSFC for the ventral part of area 6 that is involved in orofacial motor control and RSFC associated with Broca’s region (areas 44 and 45). These findings indicate rich and differential RSFC patterns for the ventrolateral frontal areas controlling language production, consistent with known anatomical connectivity in the macaque brain, and suggest conservation of connectivity during the evolution of the primate brain.

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