The organization and connections of anterior and posterior parietal cortex in titi monkeys: do New World monkeys have an area 2?

We used multiunit electrophysiological recording techniques to examine the topographic organization of somatosensory area 3b and cortex posterior to area 3b, including area 1 and the presumptive area 5, in the New World titi monkey, Callicebus moloch. We also examined the ipsilateral and contralateral connections of these fields, as well as those in a region of cortex that appeared to be similar to both area 7b and the anterior intraparietal area (7b/AIP) described in macaque monkeys. All data were combined with architectonic analysis to generate comprehensive reconstructions. These studies led to several observations. First, area 1 in titi monkeys is not as precisely organized in terms of topographic order and receptive field size as is area 1 in macaque monkeys and a few New World monkeys. Second, cortex caudal to area 1 in titi monkeys is dominated by the representation of the hand and forelimb, and contains neurons that are often responsive to visual stimulation as well as somatic stimulation. This organization is more like area 5 described in macaque monkeys than like area 2. Third, ipsilateral and contralateral cortical connections become more broadly distributed away from area 3b towards the posterior parietal cortex. Specifically, area 3b has a relatively restricted pattern of connectivity with adjacent somatosensory fields 3a, 1, S2 and PV; area 1 has more broadly distributed connections than area 3b; and the presumptive areas 5 and 7b/AIP have highly diverse connections, including connections with motor and premotor cortex, extrastriate visual areas, auditory areas and somatosensory areas of the lateral sulcus. Fourth, the hand representation of the presumptive area 5 has dense callosal connections. Our results, together with previous studies in other primates, suggest that anterior parietal cortex has expanded in some primate lineages, perhaps in relation to manual abilities, and that the region of cortex we term area 5 is involved in integrating somatic inputs with the motor system and across hemispheres. Such connections could form the substrate for intentional reaching, grasping and intermanual transfer of information necessary for bilateral coordination of the hands.

[1]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

[2]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[3]  L. Krubitzer The organization of neocortex in mammals: are species differences really so different? , 1995, Trends in Neurosciences.

[4]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[5]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[6]  D. Pandya,et al.  Cortico‐cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey , 1978, The Journal of comparative neurology.

[7]  J. Kaas,et al.  Representation of the body surface in somatic koniocortex in the prosimian Galago , 1980, The Journal of comparative neurology.

[8]  H. Sakata,et al.  From Three-Dimensional Space Vision to Prehensile Hand Movements: The Lateral Intraparietal Area Links the Area V3A and the Anterior Intraparietal Area in Macaques , 2001, The Journal of Neuroscience.

[9]  David P. Friedman,et al.  Corticocortical connections predict patches of stimulus‐evoked metabolic activity in monkey somatosensory cortex , 1990, The Journal of comparative neurology.

[10]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[11]  J. Kaas,et al.  Topography, architecture, and connections of somatosensory cortex in opossums: Evidence for five somatosensory areas , 1996, The Journal of comparative neurology.

[12]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[13]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[14]  M. Tanaka,et al.  Coding of modified body schema during tool use by macaque postcentral neurones. , 1996, Neuroreport.

[15]  D. Pandya,et al.  Homotopic and nonhomotopic interhemispheric cortical projections in the squirrel monkey. , 1971, Experimental neurology.

[16]  T. Powell,et al.  The ipsilateral cortico-cortical connections of area 7b, PF, in the parietal and tempral lobes of the monkey , 1990, Brain Research.

[17]  R B Masterton,et al.  Somatosensory and motor representations in cerebral cortex of a primitive mammal (Monodelphis domestica): A window into the early evolution of sensorimotor cortex , 2000, The Journal of comparative neurology.

[18]  J. Semmes,et al.  Behavioral consequences of selective subtotal ablations in the postcentral gyrus of Macaca mulatta. , 1974, Brain research.

[19]  R H LaMotte,et al.  Disorders in somesthesis following lesions of parietal lobe. , 1979, Journal of neurophysiology.

[20]  M. Sur,et al.  Representations of the body surface in postcentral parietal cortex of Macaca fascicularis , 1980, The Journal of comparative neurology.

[21]  Takashi Toda,et al.  Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex , 1998, Experimental Brain Research.

[22]  M. Carlson,et al.  Characteristics of sensory deficits following lesions of brodmann's areas 1 and 2 in the postcentral gyrus ofMacaca mulatta , 1981, Brain Research.

[23]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[24]  Juhani Hyvärinen,et al.  Distribution of visual and somatic functions in the parietal associative area 7 of the monkey , 1979, Brain Research.

[25]  M. Taoka,et al.  The complexity of receptive fields of periodontal mechanoreceptive neurons in the postcentral area 2 of conscious macaque monkey brains. , 2001, Archives of oral biology.

[26]  J. Hyvärinen,et al.  Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. , 1974, Brain : a journal of neurology.

[27]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[28]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[29]  J. Kaas,et al.  Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: Comparisons with other primates , 1982, The Journal of comparative neurology.

[30]  R Caminiti,et al.  The callosal system of the superior parietal lobule in the monkey , 1985, The Journal of comparative neurology.

[31]  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.

[32]  Leah Krubitzer,et al.  Organization of sensory cortex in a Madagascan insectivore, the tenrec (Echinops telfairi) , 1997, The Journal of comparative neurology.

[33]  E P Gardner,et al.  Somatosensory cortical mechanisms of feature detection in tactile and kinesthetic discrimination. , 1988, Canadian journal of physiology and pharmacology.

[34]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[35]  J. Eisenberg,et al.  The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation, and Behavior , 1981 .

[36]  T. P. S. Powell,et al.  The cortico-cortical connections of area 7b, PF, in the parietal lobe of the monkey , 1987, Brain Research.

[37]  W. Murphy,et al.  Resolution of the Early Placental Mammal Radiation Using Bayesian Phylogenetics , 2001, Science.

[38]  L. Krubitzer,et al.  Organization of somatosensory cortex in three species of marsupials, Dasyurus hallucatus, Dactylopsila trivirgata, and Monodelphis domestica: Neural correlates of morphological specializations , 1999, The Journal of comparative neurology.

[39]  J. Kaas,et al.  Double representation of the body surface within cytoarchitectonic area 3b and 1 in “SI” in the owl monkey (aotus trivirgatus) , 1978, The Journal of comparative neurology.

[40]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[41]  M. Marzke,et al.  Evolution of the human hand: approaches to acquiring, analysing and interpreting the anatomical evidence , 2000, Journal of anatomy.

[42]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  A M Dale,et al.  Segregation of somatosensory activation in the human rolandic cortex using fMRI. , 2000, Journal of neurophysiology.

[44]  R. LaMotte,et al.  Fine-scale organization of SI (area 3b) in the squirrel monkey revealed with intrinsic optical imaging. , 2001, Journal of neurophysiology.

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

[46]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[47]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

[48]  J. Kaas,et al.  Representations of the body surface in areas 3b and 1 of postcentral parietal cortex of cebus monkeys , 1983, Brain Research.

[49]  D. Pandya,et al.  Interhemispheric neocortical projections of somatosensory areas I and II in the rhesus monkey. , 1968, Brain research.

[50]  Leah Krubitzer,et al.  Interhemispheric connections of somatosensory cortex in the flying fox , 1998, The Journal of comparative neurology.

[51]  L. Krubitzer,et al.  Five topographically organized fields in the somatosensory cortex of the flying fox: Microelectrode maps, myeloarchitecture, and cortical modules , 1992, The Journal of comparative neurology.

[52]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[53]  L. Bianchi,et al.  Posterior parietal cortex: functional properties of neurons in area 5 during an instructed-delay reaching task within different parts of space , 2004, Experimental Brain Research.

[54]  H Burton,et al.  Neuronal activity in the primary somatosensory cortex in monkeys (Macaca mulatta) during active touch of textured surface gratings: responses to groove width, applied force, and velocity of motion. , 1991, Journal of neurophysiology.

[55]  T. P. S. Powell,et al.  The callosal connexions of the primary somatic sensory cortex in the monkey , 1985, Brain Research Reviews.

[56]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  S. Scott,et al.  Cortical control of reaching movements , 1997, Current Opinion in Neurobiology.

[58]  D. Pandya,et al.  The distribution of the corpus callosum in the Rhesus monkey. , 1971, Brain : a journal of neurology.

[59]  E. G. Jones,et al.  Commissural and cortico-cortical "columns" in the somatic sensory cortex of primates , 1975, Science.

[60]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[61]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[62]  C. Robinson,et al.  Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis , 1980, The Journal of comparative neurology.

[63]  W. Jiang,et al.  Neuronal encoding of texture changes in the primary and the secondary somatosensory cortical areas of monkeys during passive texture discrimination. , 1997, Journal of neurophysiology.

[64]  C. E. Chapman,et al.  Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task , 2004, Experimental Brain Research.

[65]  J. Kaas,et al.  Connections of primary auditory cortex in the new world monkey, Saguinus , 1989, The Journal of comparative neurology.

[66]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[67]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[68]  J Hyvärinen,et al.  Receptive field integration and submodality convergence in the hand area of the post‐central gyrus of the alert monkey. , 1978, The Journal of physiology.

[69]  J. Hyvärinen,et al.  I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys , 1979, Experimental Brain Research.

[70]  M. Tanaka,et al.  Processing of tactile and kinesthetic signals from bilateral sides of the body in the postcentral gyrus of awake monkeys , 2002, Behavioural Brain Research.

[71]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

[72]  B Bioulac,et al.  A quantitative study of neuronal discharge in areas 5, 2, and 4 of the monkey during fast arm movements. , 1991, Journal of neurophysiology.

[73]  J. Saver,et al.  A Quantitative Study , 2005 .

[74]  J. W. Neal The callosal connections of area 7b, PF in the monkey , 1990, Brain Research.

[75]  L. Krubitzer,et al.  Multiple somatosensory areas in the anterior parietal cortex of the California ground squirrel (Spermophilus beecheyii) , 2000, The Journal of comparative neurology.

[76]  C. Darian‐Smith,et al.  Ipsilateral cortical projections to areas 3a, 3b, and 4 in the macaque monkey , 1993, The Journal of comparative neurology.

[77]  L. Pubols,et al.  Somatotopic organization of spider monkey somatic sensory cerebral cortex , 1971, The Journal of comparative neurology.

[78]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. , 1969, Brain : a journal of neurology.

[79]  Atsushi Iriki,et al.  Self-images in the video monitor coded by monkey intraparietal neurons , 2001, Neuroscience Research.

[80]  J. Johnson Comparative Development of Somatic Sensory Cortex , 1990 .

[81]  O. Grüsser,et al.  Cortico‐cortical connections and cytoarchitectonics of the primate vestibular cortex: A study in squirrel monkeys (Saimiri sciureus) , 1992, The Journal of comparative neurology.

[82]  J. Kaas,et al.  Studies on the evolution of multiple somatosensory representations in primates: The organization of anterior parietal cortex in the new world callitrichid, Saguinus , 1986, The Journal of comparative neurology.

[83]  Esther P. Gardner,et al.  Comparison of neuronal firing rates in somatosensory and posterior parietal cortex during prehension , 2001, Experimental Brain Research.

[84]  Atsushi Iriki,et al.  Bilateral receptive field neurons in the hindlimb region of the postcentral somatosensory cortex in awake macaque monkeys , 2000, Experimental Brain Research.

[85]  Leah Krubitzer,et al.  Organization of area 3a in macaque monkeys: Contributions to the cortical phenotype , 2004, The Journal of comparative neurology.

[86]  C. Cavada,et al.  The Visual Parietal Areas in the Macaque Monkey: Current Structural Knowledge and Ignorance , 2001, NeuroImage.

[87]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[88]  M. Raichle,et al.  Mapping human somatosensory cortex with positron emission tomography. , 1987, Journal of neurosurgery.

[89]  P E Roland,et al.  Astereognosis. Tactile discrimination after localized hemispheric lesions in man. , 1976, Archives of neurology.

[90]  F. Lacquaniti,et al.  Representing spatial information for limb movement: role of area 5 in the monkey. , 1995, Cerebral cortex.

[91]  C E Chapman,et al.  Cortical mechanisms underlying tactile discrimination in the monkey. I. Role of primary somatosensory cortex in passive texture discrimination. , 1996, Journal of neurophysiology.

[92]  J. Napier,et al.  The evolution of the hand. , 1962, Scientific American.

[93]  S P Wise,et al.  Size, laminar and columnar distribution of efferent cells in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[94]  L Krubitzer,et al.  Area 3a: topographic organization and cortical connections in marmoset monkeys. , 2001, Cerebral cortex.

[95]  Y. Iwamura,et al.  Bilateral receptive field neurons and callosal connections in the somatosensory cortex. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[96]  Leah Krubitzer,et al.  Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys , 2003, The Journal of comparative neurology.

[97]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[98]  T. P. S. Powell,et al.  The organization of the corticocortical projection of area 5 upon area 7 in the parietal lobe of the monkey , 1986, Brain Research.

[99]  Mara Fabri,et al.  Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys , 1995, The Journal of comparative neurology.

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

[101]  S P Wise,et al.  Commissural columns in the sensory‐motor cortex of monkeys , 1979, The Journal of comparative neurology.

[102]  A. S. Schwartz Functional relationship between somatosensory cortex and specialized afferent pathways in the monkey , 1983, Experimental Neurology.

[103]  Integration of the upper and lower lips in the postcentral area 2 of conscious macaque monkeys (Macaca fuscata). , 2002, Archives of oral biology.

[104]  H. Killackey,et al.  Organization of corticocortical connections in the parietal cortex of the rat , 1978, The Journal of comparative neurology.

[105]  A. Grinvald,et al.  The Cortical Representation of the Hand in Macaque and Human Area S-I: High Resolution Optical Imaging , 2001, The Journal of Neuroscience.

[106]  J. Hyvärinen Posterior parietal lobe of the primate brain. , 1982, Physiological reviews.

[107]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[108]  H. Sakata,et al.  Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. , 1995, Cerebral cortex.

[109]  Jon H Kaas,et al.  Somatosensory cortex of prosimian Galagos: Physiological recording, cytoarchitecture, and corticocortical connections of anterior parietal cortex and cortex of the lateral sulcus , 2003, The Journal of comparative neurology.

[110]  Neeraj Jain,et al.  Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys , 2001, The Journal of comparative neurology.

[111]  C. E. Chapman,et al.  Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task , 2004, Experimental Brain Research.