Intrinsic functional clustering of ventral premotor F5 in the macaque brain

Neurophysiological and anatomical data suggest the existence of several functionally distinct regions in the lower arcuate sulcus and adjacent postarcuate convexity of the macaque monkey. Ventral premotor F5c lies on the postarcuate convexity and consists of a dorsal hand-related and ventral mouth-related field. The posterior bank of the lower arcuate contains two additional premotor F5 subfields at different anterior-posterior levels, F5a and F5p. Anterior to F5a, area 44 has been described as a dysgranular zone occupying the deepest part of the fundus of the inferior arcuate. Finally, area GrFO occupies the most rostral portion of the fundus and posterior bank of inferior arcuate and extends ventrally onto the frontal operculum. Recently, data-driven exploratory approaches using resting-state fMRI data have been suggested as a promising non-invasive method for examining the functional organization of the primate brain. Here, we examined to what extent partitioning schemes derived from data driven clustering analysis of resting-state fMRI data correspond with the proposed organization of the fundus and posterior bank of the macaque arcuate sulcus, as suggested by invasive architectonical, connectional and functional investigations. Using a hierarchical clustering analysis, we could retrieve clusters corresponding to the dorsal and ventral portions of F5c on the postarcuate convexity, F5a and F5p at different antero-posterior locations on the posterior bank of the lower arcuate, area 44 in the fundus, as well as part of area GrFO in the most anterior portion of the fundus. Additionally, each of these clusters displayed distinct whole-brain functional connectivity, in line with previous anatomical tracer and seed-based functional connectivity investigations of F5/44 subdivisions. Overall, our data suggests that hierarchical clustering analysis of resting-state fMRI data can retrieve a fine-grained level of cortical organization that resembles detailed parcellation schemes derived from invasive functional and anatomical investigations.

[1]  K. Zilles,et al.  Differences in cytoarchitecture of Broca's region between human, ape and macaque brains , 2019, Cortex.

[2]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[3]  Andreas Nieder,et al.  Audio-Vocal Interaction in Single Neurons of the Monkey Ventrolateral Prefrontal Cortex , 2015, The Journal of Neuroscience.

[4]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[5]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.

[6]  Anatomical and functional subdivisions of inferior area 6 in macaque monkey , 1996 .

[7]  Dante Mantini,et al.  Functional specialization of macaque premotor F5 subfields with respect to hand and mouth movements: A comparison of task and resting-state fMRI , 2019, NeuroImage.

[8]  Pierpaolo Pani,et al.  Selectivity for Three-Dimensional Shape and Grasping-Related Activity in the Macaque Ventral Premotor Cortex , 2012, The Journal of Neuroscience.

[9]  Elena Borra,et al.  Functional anatomy of the macaque temporo-parieto-frontal connectivity , 2017, Cortex.

[10]  W Pieter Medendorp,et al.  Mapping multiple principles of parietal–frontal cortical organization using functional connectivity , 2018, Brain Structure and Function.

[11]  Wim Vanduffel,et al.  Decoding Grasping Movements from the Parieto-Frontal Reaching Circuit in the Nonhuman Primate , 2018, Cerebral cortex.

[12]  Stefan Everling,et al.  Functional subdivisions of medial parieto-occipital cortex in humans and nonhuman primates using resting-state fMRI , 2015, NeuroImage.

[13]  Guy A. Orban,et al.  The monkey ventral premotor cortex processes 3D shape from disparity , 2009, NeuroImage.

[14]  Marzio Gerbella,et al.  Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex , 2009, The Journal of comparative neurology.

[15]  Ravi S. Menon,et al.  Divergence of rodent and primate medial frontal cortex functional connectivity , 2020, Proceedings of the National Academy of Sciences.

[16]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[17]  Ravi S. Menon,et al.  Frontoparietal Functional Connectivity in the Common Marmoset , 2016, Cerebral cortex.

[18]  Liang Wang,et al.  Intrinsic connectivity between the hippocampus and posteromedial cortex predicts memory performance in cognitively intact older individuals , 2010, NeuroImage.

[19]  Monica Maranesi,et al.  Anatomo‐functional organization of the ventral primary motor and premotor cortex in the macaque monkey , 2012, The European journal of neuroscience.

[20]  G. Rizzolatti,et al.  Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey , 1985, Behavioural Brain Research.

[21]  Elena Borra,et al.  Computational Architecture of the Parieto-Frontal Network Underlying Cognitive-Motor Control in Monkeys , 2017, eNeuro.

[22]  Dante Mantini,et al.  A ventral salience network in the macaque brain , 2016, NeuroImage.

[23]  G. Luppino,et al.  Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5 , 2011, Brain Structure and Function.

[24]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[25]  Andreas Nieder,et al.  Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations , 2013, Nature Communications.

[26]  Vivek Prabhakaran,et al.  The effect of resting condition on resting-state fMRI reliability and consistency: A comparison between resting with eyes open, closed, and fixated , 2013, NeuroImage.

[27]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[28]  Joseph S. Gati,et al.  Intrinsic functional clustering of anterior cingulate cortex in the common marmoset , 2019, NeuroImage.

[29]  G. Orban,et al.  Default Mode of Brain Function in Monkeys , 2011, The Journal of Neuroscience.

[30]  M. Petrides,et al.  Cortico-cortical connections of areas 44 and 45B in the macaque monkey , 2014, Brain and Language.

[31]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[32]  G. Luppino,et al.  Connections of the macaque Granular Frontal Opercular (GrFO) area: a possible neural substrate for the contribution of limbic inputs for controlling hand and face/mouth actions , 2014, Brain Structure and Function.

[33]  G. Orban,et al.  Observing Others: Multiple Action Representation in the Frontal Lobe , 2005, Science.

[34]  Elena Borra,et al.  Reproducing macaque lateral grasping and oculomotor networks using resting state functional connectivity and diffusion tractography , 2020, Brain structure & function.

[35]  M. Petrides,et al.  Orofacial somatomotor responses in the macaque monkey homologue of Broca's area , 2005, Nature.

[36]  Ravi S. Menon,et al.  Resting-state connectivity identifies distinct functional networks in macaque cingulate cortex. , 2012, Cerebral cortex.

[37]  M. Gerbella,et al.  Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways , 2017, Neuroscience.

[38]  W. Vanduffel,et al.  Visual Field Map Clusters in Macaque Extrastriate Visual Cortex , 2009, The Journal of Neuroscience.

[39]  Stefan Everling,et al.  Broad intrinsic functional connectivity boundaries of the macaque prefrontal cortex , 2014, NeuroImage.

[40]  Stephen V. Shepherd,et al.  Functional Networks for Social Communication in the Macaque Monkey , 2018, Neuron.

[41]  G. Rizzolatti,et al.  ß Federation of European Neuroscience Societies Mirror , 2003 .

[42]  Joseph S. Gati,et al.  Intrinsic Functional Boundaries of Lateral Frontal Cortex in the Common Marmoset Monkey , 2018, The Journal of Neuroscience.

[43]  Marzio Gerbella,et al.  The macaque lateral grasping network: A neural substrate for generating purposeful hand actions , 2017, Neuroscience & Biobehavioral Reviews.

[44]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[45]  Matthew F.S. Rushworth,et al.  Comparing brains by matching connectivity profiles , 2016, Neuroscience & Biobehavioral Reviews.

[46]  Adam G. Thomas,et al.  Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas in Monkey Frontal Cortex , 2014, Neuron.

[47]  Ravi S. Menon,et al.  Functional connectivity of the frontal eye fields in humans and macaque monkeys investigated with resting-state fMRI. , 2012, Journal of neurophysiology.

[48]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[49]  Wim Vanduffel,et al.  Grasping-Related Functional Magnetic Resonance Imaging Brain Responses in the Macaque Monkey , 2011, The Journal of Neuroscience.

[50]  Stefan Everling,et al.  Intrinsic functional architecture of the macaque dorsal and ventral lateral frontal cortex , 2016, bioRxiv.

[51]  V. Calhoun,et al.  Resting state connectivity differences in eyes open versus eyes closed conditions , 2019, Human brain mapping.