Cortical input to the frontal pole of the marmoset monkey.

We used fluorescent tracers to map the pattern of cortical afferents to frontal area 10 in marmosets. Dense projections originated in several subdivisions of orbitofrontal cortex, in the medial frontal cortex (particularly areas 14 and 32), and in the dorsolateral frontal cortex (particularly areas 8Ad and 9). Major projections also stemmed, in variable proportions depending on location of the injection site, from both the inferior and superior temporal sensory association areas, suggesting a degree of audiovisual convergence. Other temporal projections included the superior temporal polysensory cortex, temporal pole, and parabelt auditory cortex. Medial area 10 received additional projections from retrosplenial, rostral calcarine, and parahippocampal areas, while lateral area 10 received small projections from the ventral somatosensory and premotor areas. There were no afferents from posterior parietal or occipital areas. Most frontal connections were balanced in terms of laminar origin, giving few indications of an anatomical hierarchy. The pattern of frontopolar afferents suggests an interface between high-order representations of the sensory world and internally generated states, including working memory, which may subserve ongoing evaluation of the consequences of decisions as well as other cognitive functions. The results also suggest the existence of functional differences between subregions of area 10.

[1]  Masatoshi Itoh,et al.  Thinking of the future and past: the roles of the frontal pole and the medial temporal lobes , 2003, NeuroImage.

[2]  Stephanie Spengler,et al.  Differential functions of lateral and medial rostral prefrontal cortex (area 10) revealed by brain-behavior associations. , 2005, Cerebral cortex.

[3]  A M Galaburda,et al.  The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey , 1983, The Journal of comparative neurology.

[4]  A. Morel,et al.  Connections of visual areas of the upper temporal lobe of owl monkeys: the MT crescent and dorsal and ventral subdivisions of FST , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Thomas H. B. FitzGerald,et al.  The Role of Human Orbitofrontal Cortex in Value Comparison for Incommensurable Objects , 2009, The Journal of Neuroscience.

[6]  A. Calder,et al.  Neural mechanisms of social attention , 2009, Trends in Cognitive Sciences.

[7]  R E Weller,et al.  Subdivisions and connections of inferior temporal cortex in owl monkeys , 1987, The Journal of comparative neurology.

[8]  K. Saleem,et al.  Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey , 2008, The Journal of comparative neurology.

[9]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[10]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[11]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[12]  H. Kennedy,et al.  Laminar Distribution of Neurons in Extrastriate Areas Projecting to Visual Areas V1 and V4 Correlates with the Hierarchical Rank and Indicates the Operation of a Distance Rule , 2000, The Journal of Neuroscience.

[13]  H. Kennedy,et al.  Anatomical Evidence of Multimodal Integration in Primate Striate Cortex , 2002, The Journal of Neuroscience.

[14]  Hideki Kondo,et al.  Differential connections of the temporal pole with the orbital and medial prefrontal networks in macaque monkeys , 2003, The Journal of comparative neurology.

[15]  David H Zald,et al.  Neural correlates of tasting concentrated quinine and sugar solutions. , 2002, Journal of neurophysiology.

[16]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[17]  M. Abercrombie Estimation of nuclear population from microtome sections , 1946, The Anatomical record.

[18]  P. Goldman-Rakic,et al.  Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates , 1991, The Journal of comparative neurology.

[19]  T. Insel,et al.  Differential expansion of neural projection systems in primate brain evolution. , 1999, Neuroreport.

[20]  C. Galletti,et al.  Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex , 2009, The Journal of Neuroscience.

[21]  John Q. Trojanowski,et al.  Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents , 1977, Brain Research.

[22]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[23]  L. Heimer,et al.  In vivo anterograde and retrograde axonal trnasport of the fluoresecent rhodamine-dextran-amine, Fluor-Ruby, within the CNS , 1990, Brain Research.

[24]  H. Okano,et al.  Generation of transgenic non-human primates with germline transmission , 2009, Nature.

[25]  Mario Fiorani,et al.  Parallel Evolution of Cortical Areas Involved in Skilled Hand Use , 2007, The Journal of Neuroscience.

[26]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[27]  G. Bonin,et al.  The neocortex of hapale , 1947, The Journal of comparative neurology.

[28]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[29]  Marcello G P Rosa,et al.  Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications. , 2006, Cerebral cortex.

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

[31]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[32]  P. Barone,et al.  Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey , 2005, The European journal of neuroscience.

[33]  S. Shimojo,et al.  Parcellation and Area-Area Connectivity as a Function of Neocortex Size , 2005, Brain, Behavior and Evolution.

[34]  Aldo Genovesio,et al.  Evaluating self-generated decisions in frontal pole cortex of monkeys , 2009, Nature Neuroscience.

[35]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[36]  J L Ringo,et al.  Neuronal interconnection as a function of brain size. , 1991, Brain, behavior and evolution.

[37]  L A Krubitzer,et al.  Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns , 1990, Visual Neuroscience.

[38]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[39]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[40]  D. Pandya,et al.  Efferent Association Pathways from the Rostral Prefrontal Cortex in the Macaque Monkey , 2007, The Journal of Neuroscience.

[41]  G. Luppino,et al.  Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. , 2010, Cerebral cortex.

[42]  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.

[43]  Marcello G P Rosa,et al.  Brain maps, great and small: lessons from comparative studies of primate visual cortical organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  G. Schatten,et al.  Developmental biology: Transgenic primate offspring , 2009, Nature.

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

[46]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: I. Three‐dimensional and cytoarchitectonic organization , 2000, The Journal of comparative neurology.

[47]  D. Perrett,et al.  Integration of form and motion in the anterior superior temporal polysensory area (STPa) of the macaque monkey. , 1996, Journal of neurophysiology.

[48]  Doris Y. Tsao,et al.  Patches of face-selective cortex in the macaque frontal lobe , 2008, Nature Neuroscience.

[49]  Claus C Hilgetag,et al.  Graded classes of cortical connections: quantitative analyses of laminar projections to motion areas of cat extrastriate cortex , 2005, The European journal of neuroscience.

[50]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[51]  W. K. Simmons,et al.  The Selectivity and Functional Connectivity of the Anterior Temporal Lobes , 2009, Cerebral cortex.

[52]  M. Gamberini,et al.  Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus) , 2005, The Journal of comparative neurology.

[53]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[54]  James K. Kroger,et al.  Rostrolateral Prefrontal Cortex Involvement in Relational Integration during Reasoning , 2001, NeuroImage.

[55]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

[56]  T. Braver,et al.  The Role of Frontopolar Cortex in Subgoal Processing during Working Memory , 2002, NeuroImage.

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

[58]  R. W. Guillery On counting and counting errors , 2002, The Journal of comparative neurology.

[59]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[60]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

[61]  Lisa A. de la Mothe,et al.  Thalamic connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[62]  J. Kaas The future of mapping sensory cortex in primates: three of many remaining issues , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[63]  Matthew W Spitzer,et al.  Connections of the marmoset rostrotemporal auditory area: express pathways for analysis of affective content in hearing , 2009, The European journal of neuroscience.

[64]  R. Weller,et al.  Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys , 1992, The Journal of comparative neurology.

[65]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[66]  G. Orban,et al.  Comparative mapping of higher visual areas in monkeys and humans , 2004, Trends in Cognitive Sciences.

[67]  R. Elliott,et al.  Hedonic and informational functions of the human orbitofrontal cortex. , 2010, Cerebral cortex.

[68]  J. Trojanowski,et al.  Prefrontal granular cortex of the rhesus monkey. II. Interhemispheric cortical afferents , 1977, Brain Research.

[69]  Jon H Kaas,et al.  Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch) , 2004, The Journal of comparative neurology.

[70]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: III. Cortical efferents , 2003, The Journal of comparative neurology.

[71]  Kathleen J. Burman,et al.  Architectural subdivisions of medial and orbital frontal cortices in the marmoset monkey (Callithrix jacchus) , 2009, The Journal of comparative neurology.

[72]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[73]  F. Condé Further studies on the use of the fluorescent tracers fast blue and diamidino yellow: Effective uptake area and cellular storage sites , 1987, Journal of Neuroscience Methods.

[74]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[75]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[76]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[77]  Michela Gamberini,et al.  Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas , 2006, The Journal of comparative neurology.

[78]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[79]  Trevor W Robbins,et al.  Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): An anterograde and retrograde tract‐tracing study , 2007, The Journal of comparative neurology.

[80]  H. Barbas,et al.  Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey , 2005, BMC Neuroscience.

[81]  P. Clarke How inaccurate is the Abercrombie correction factor for cell counts? , 1992, Trends in Neurosciences.

[82]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[83]  H. Kuypers,et al.  Diamidino yellow dihydrochloride (DY·2HCl); a new fluorescent retrograde neuronal tracer, which migrates only very slowly out of the cell , 2004, Experimental Brain Research.

[84]  A. Damasio,et al.  The return of Phineas Gage: clues about the brain from the skull of a famous patient. , 1994, Science.

[85]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[86]  B. Seltzer,et al.  Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex , 1995, The Journal of comparative neurology.

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

[88]  K. Saleem,et al.  Differential connections of the perirhinal and parahippocampal cortex with the orbital and medial prefrontal networks in macaque monkeys , 2005, The Journal of comparative neurology.

[89]  Matthew W Spitzer,et al.  Anatomical and physiological definition of the motor cortex of the marmoset monkey , 2008, The Journal of comparative neurology.

[90]  H. Barbas,et al.  Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey , 1993, Neuroscience.

[91]  M. Feinberg,et al.  Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in primates. , 2007, Cerebral cortex.

[92]  Yoshinao Kajikawa,et al.  Cortical connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[93]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[94]  M. Rosa,et al.  Visual areas in lateral and ventral extrastriate cortices of the marmoset monkey , 2000, The Journal of comparative neurology.

[95]  D. Perrett,et al.  Neural Representation for the Perception of the Intentionality of Actions , 2000, Brain and Cognition.

[96]  Roberta L. Klatzky,et al.  What vs. where in touch: an fMRI study , 2005, NeuroImage.

[97]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[98]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

[99]  M. Rosa,et al.  A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision , 2006, The European journal of neuroscience.

[100]  M. Rosa Visual maps in the adult primate cerebral cortex: some implications for brain development and evolution. , 2002, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.