Subcortical projections to the frontal pole in the marmoset monkey

The subcortical projections to the marmoset frontal pole were mapped with the use of fluorescent tracer injections. The main thalamic projections, which originated in both the magnocellular and parvocellular subdivisions of the mediodorsal nucleus, were topographically organized. Our results suggest the existence of a third, caudal subdivision of this nucleus, which is likely to be homologous to the macaque’s pars densocellularis. A substantial, but not topographically organized, projection to Brodmann’s area 10 originated in the medial part of the ventral anterior nucleus. Minor thalamic projections originated in the medial pulvinar nucleus and in the midline/intralaminar nuclei. Finally, the posterior thalamic group (including the limitans and suprageniculate nuclei) sent a small projection to rostral area 10 that has not previously been documented in primates. The main extrathalamic projections stemmed from the claustrum, which contained as many as 50% of all subcortical labelled neurons. Minor connections originated in the hypothalamus (mainly in the lateral anterior and lateral tuberal regions), dorsal periaqueductal grey matter, basal forebrain (nucleus basalis of Meynert and horizontal limb of the diagonal band of Broca), and amygdala (basal, accessory basal and lateral nuclei). The present results, combined with recent data on the cortical projections to area 10, reveal the frontal pole as a region that integrates information from multiple neural processing systems, including high‐level sensory, limbic and working memory‐related structures. Although the pattern of subcortical projections is similar to that previously described in the macaque, suggesting a homologous organization, the present data also suggest functional distinctions between medial and lateral sectors of area 10.

[1]  Leslie G. Ungerleider,et al.  Thalamic and temporal cortex input to medial prefrontal cortex in rhesus monkeys , 1997, Experimental Brain Research.

[2]  J. Price,et al.  Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in Macaque monkeys , 1998, The Journal of comparative neurology.

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

[4]  Hans J. Markowitsch,et al.  Thalamic mediodorsal nucleus and memory: A critical evaluation of studies in animals and man , 1982, Neuroscience & Biobehavioral Reviews.

[5]  D. Xiaob,et al.  Pathways for emotions and memory II . Afferent input to the anterior thalamic nuclei from prefrontal , temporal , hypothalamic areas and the basal ganglia in the rhesus monkey , 2002 .

[6]  J. W. Papez A PROPOSED MECHANISM OF EMOTION , 1937 .

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

[8]  G. Leichnetz,et al.  Efferent connections of the orbitofrontal cortex in the marmoset(Saguinus oedipus) , 1975, Brain Research.

[9]  O. Creutzfeldt,et al.  The second, intralaminar thalamo-cortical projection system , 2004, Anatomy and Embryology.

[10]  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.

[11]  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.

[12]  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.

[13]  Amanda Parker,et al.  The effect of anterior thalamic and cingulate cortex lesions on object-in-place memory in monkeys , 1997, Neuropsychologia.

[14]  H. Barbas,et al.  Diverse thalamic projections to the prefrontal cortex in the rhesus monkey , 1991, The Journal of comparative neurology.

[15]  H. Barbas,et al.  Pathways for emotions and memory: I. Input and output zones linking the anterior thalamic nuclei with prefrontal cortices in the rhesus monkey , 2002 .

[16]  D. Boussaoud,et al.  Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey , 2002, The Journal of comparative neurology.

[17]  T. Robbins,et al.  Differential Contributions of the Primate Ventrolateral Prefrontal and Orbitofrontal Cortex to Serial Reversal Learning , 2010, The Journal of Neuroscience.

[18]  H. Pape,et al.  Direct synaptic connections of axons from superior colliculus with identified thalamo‐amygdaloid projection neurons in the rat: Possible substrates of a subcortical visual pathway to the amygdala , 1999, The Journal of comparative neurology.

[19]  D. Amaral,et al.  Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study , 2002, The Journal of comparative neurology.

[20]  John Q. Trojanowski,et al.  Amygdaloid projections to prefrontal granular cortex in rhesus monkey demonstrated with horseradish peroxidase , 1975, Brain Research.

[21]  H. Barbas,et al.  Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey , 2001, Neuroscience.

[22]  H. Barbas,et al.  Organization of afferent input to subdivisions of area 8 in the rhesus monkey , 1981, The Journal of comparative neurology.

[23]  D. Amaral,et al.  Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala: A retrograde tracing study , 2000, The Journal of comparative neurology.

[24]  R. Bandler,et al.  Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. , 1996, Progress in brain research.

[25]  T. Robbins,et al.  Distribution and some projections of cholinergic neurons in the brain of the common marmoset, Callithrix jacchus , 1988, The Journal of comparative neurology.

[26]  H. Barbas,et al.  Prefrontal Projections to the Thalamic Reticular Nucleus form a Unique Circuit for Attentional Mechanisms , 2006, The Journal of Neuroscience.

[27]  J. Olszewski The Thalamus of the Macaca Mulatta: An Atlas for Use with the Stereotaxic Instrument , 1952 .

[28]  L. P. Morin,et al.  Neuropeptide Y and enkephalin immunoreactivity in retinorecipient nuclei of the hamster pretectum and thalamus , 1997, Visual Neuroscience.

[29]  O. Creutzfeldt,et al.  The topology of the thalamo-cortical projections in the marmoset monkey (Callithrix jacchus) , 2004, Experimental Brain Research.

[30]  A. Roberts,et al.  Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[31]  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.

[32]  Philip G. F. Browning,et al.  Neurotoxic Lesions of the Medial Mediodorsal Nucleus of the Thalamus Disrupt Reinforcer Devaluation Effects in Rhesus Monkeys , 2007, The Journal of Neuroscience.

[33]  J. Price,et al.  Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys , 2007, The Journal of comparative neurology.

[34]  A. Roberts,et al.  Autonomic, behavioral, and neural analyses of mild conditioned negative affect in marmosets. , 2010, Behavioral neuroscience.

[35]  J. Baizer,et al.  Projections from the claustrum to the prelunate gyrus in the monkey , 1997, Experimental Brain Research.

[36]  J. K. Harting,et al.  Ascending pathways from the monkey superior colliculus: An autoradiographic analysis , 1980, The Journal of comparative neurology.

[37]  P. Goldman-Rakic,et al.  Organization of the nigrothalamocortical system in the rhesus monkey , 1985, The Journal of comparative neurology.

[38]  K. Kultas‐Ilinsky,et al.  Fine structure of the magnocellular subdivision of the ventral anterior thalamic nucleus (V Amc) of Macaca mulatta: II. Organization of nigrothalamic afferents as revealed with EM autoradiography , 1990, The Journal of comparative neurology.

[39]  T. Robbins,et al.  Differential effects of 6-OHDA lesions of the frontal cortex and caudate nucleus on the ability to acquire an attentional set. , 2001, Cerebral cortex.

[40]  H. Barbas,et al.  Circuits through prefrontal cortex, basal ganglia, and ventral anterior nucleus map pathways beyond motor control , 2004 .

[41]  Hsin-Hao Yu,et al.  Cortical input to the frontal pole of the marmoset monkey. , 2011, Cerebral cortex.

[42]  H. Barbas,et al.  Topographic Organization of Connections between the Hypothalamus and Prefrontal Cortex in the Rhesus Monkey , 2022 .

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

[44]  R. Dampney,et al.  Modulation of the baroreceptor reflex by the dorsomedial hypothalamic nucleus and perifornical area. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[45]  P S Goldman-Rakic,et al.  Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey , 1997, The Journal of comparative neurology.

[46]  B. Everitt,et al.  Lesions of the Orbitofrontal but not Medial Prefrontal Cortex Disrupt Conditioned Reinforcement in Primates , 2003, The Journal of Neuroscience.

[47]  D. Pandya,et al.  Prefrontal projections to the mediodorsal nucleus of the thalamus in the rhesus monkey , 1991, The Journal of comparative neurology.

[48]  M. Colonnier,et al.  Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study , 1977, The Journal of comparative neurology.

[49]  T. Wichmann,et al.  Neuronal activity in the primate substantia nigra pars reticulata during the performance of simple and memory-guided elbow movements. , 2004, Journal of neurophysiology.

[50]  M. Mesulam,et al.  Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex , 1976, Brain Research.

[51]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[52]  A. Graybiel,et al.  Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  P. Goldman-Rakic,et al.  The primate mediodorsal (MD) nucleus and its projection to the frontal lobe , 1985, The Journal of comparative neurology.

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

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

[56]  Ikuko Tanaka,et al.  Web-accessible digital brain atlas of the common marmoset (Callithrix jacchus) , 2009, Neuroscience Research.

[57]  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.

[58]  Dr. Heinz Stephan,et al.  The Brain of the Common Marmoset (Callithrix jacchus) , 1980, Springer Berlin Heidelberg.

[59]  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.

[60]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[61]  G. Kovács,et al.  Visual, somatosensory, auditory and nociceptive modality properties in the feline suprageniculate nucleus , 1997, Neuroscience.

[62]  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.

[63]  C. Geula,et al.  Cyto- and Chemoarchitecture of Basal Forebrain Cholinergic Neurons in the Common Marmoset (Callithrix Jacchus) , 2000, Experimental Neurology.

[64]  Pascal Carrive,et al.  The periaqueductal gray and defensive behavior: Functional representation and neuronal organization , 1993, Behavioural Brain Research.

[65]  T. Robbins,et al.  Prefrontal Serotonin Depletion Affects Reversal Learning But Not Attentional Set Shifting , 2005, The Journal of Neuroscience.

[66]  Giuseppe Luppino,et al.  Thalamic input to mesial and superior area 6 in the macaque monkey , 1996, The Journal of comparative neurology.

[67]  D. Mitchell The nexus between decision making and emotion regulation: A review of convergent neurocognitive substrates , 2011, Behavioural Brain Research.

[68]  T. Robbins,et al.  Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. , 2006, Cerebral cortex.

[69]  D. Gaffan,et al.  Mediodorsal thalamic function in scene memory in rhesus monkeys. , 2000, Brain : a journal of neurology.

[70]  D. Xiao,et al.  Laminar and modular organization of prefrontal projections to multiple thalamic nuclei , 2009, Neuroscience.

[71]  T. Robbins,et al.  Dissociation in prefrontal cortex of affective and attentional shifts , 1996, Nature.

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

[73]  Edilson Ervolino,et al.  Cyto-, myelo- and chemoarchitecture of the prefrontal cortex of the Cebus monkey , 2011, BMC Neuroscience.

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

[75]  L. Britto,et al.  Retinal projections to the midline and intralaminar thalamic nuclei in the common marmoset (Callithrix jacchus) , 2005, Brain Research.

[76]  J. Price,et al.  The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[77]  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.

[78]  C. Cavada,et al.  Acetylcholinesterase histochemistry in the macaque thalamus reveals territories selectively connected to frontal, parietal and temporal association cortices , 1995, Journal of Chemical Neuroanatomy.

[79]  A. Levey,et al.  Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey , 1983, The Journal of comparative neurology.

[80]  H. Kuypers,et al.  Organization of the thalamo-cortical connexions to the frontal lobe in the rhesus monkey , 1977, Experimental Brain Research.

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

[82]  S M Hilton,et al.  The hypothalamic and brainstem areas from which the cardiovascular and behavioural components of the defence reaction are elicited in the rat. , 1986, Journal of the autonomic nervous system.

[83]  N. Mizuno,et al.  Direct projections from the extrathalamic forebrain structures to the neocortex in the macaque monkey , 1982, Neuroscience Letters.

[84]  Timothy Edward John Behrens,et al.  How Green Is the Grass on the Other Side? Frontopolar Cortex and the Evidence in Favor of Alternative Courses of Action , 2009, Neuron.

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