Neurochemical and connectional organization of the dorsal pulvinar complex in monkeys

To investigate the organization of the dorsal pulvinar complex, patterns of neurochemical staining were correlated with cortico‐pulvinar connections in macaques (Macaca mulatta). Three major neurochemical subdivisions of the dorsal pulvinar were identified by acetylcholinesterase (AChE) histochemistry, as well as immunostaining for calbindin‐D28K and parvalbumin. The dorsal lateral pulvinar nucleus (PLd) was defined on histochemical criteria as a distinct AChE‐ and parvalbumin‐dense, calbindin‐poor wedge that was found to continue caudally along the dorsolateral edge of the pulvinar to within 1 mm of its caudal pole. The ventromedial border of neurochemical PLd with the rest of the dorsal pulvinar, termed the medial pulvinar (PM), was sharply defined. Overall, PM was lighter than PLd for AChE and parvalbumin and displayed lateral (PMl) and medial (PMm) histochemical divisions. PMm contained a central “oval” (PMm‐c) that stained darker for AChE and parvalbumin than the surrounding region. The neurochemically defined PLd was labeled by tracer injections in the inferior parietal lobule (IPL) and dorsolateral prefrontal cortex but not the superior temporal gyrus (STG). Label within PMl was found after prefrontal and IPL and, to a lesser extent, after STG injections. The PMm was labeled after injections of the IPL and STG, but only sparsely following prefrontal injections. The histochemically distinct subregion or module of PMm, PMm‐c, was labeled only by STG injections. Overlapping labeling was found in dorsal pulvinar divisions PMl and PLd following paired IPL/prefrontal, but not IPL/STG or these particular STG/prefrontal, injections. Thus, PLd may be a visuospatially related region whereas PM appears to contain several types of territories, some related to visual or auditory inputs, and others that receive directly converging input from posterior parietal and prefrontal cortex and may participate in a distributed cortical network concerned with visuospatial functions. J. Comp. Neurol. 419:61–86, 2000. © 2000 Wiley‐Liss, Inc.

[1]  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.

[2]  D. V. Essen,et al.  Neural mechanisms of form and motion processing in the primate visual system , 1994, Neuron.

[3]  Shraga Hocherman,et al.  Auditory- and movement-related neural activity interact in the pulvinar of the behaving rhesus monkey , 1987, Brain Research.

[4]  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.

[5]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[6]  J. Kaas,et al.  Thalamocortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[7]  A. Hendrickson,et al.  The structural organization of the inferior and lateral subdivision of the Macaca monkey pulvinar , 1979, The Journal of comparative neurology.

[8]  A. Hendrickson,et al.  Pathways between striate cortex and subcortical regions in Macaca mulatta and Saimiri sciureus: Evidence for a reciprocal pulvinar connection , 1976, Experimental Neurology.

[9]  H. Gould,et al.  Connections between area 3b of the somatosensory cortex and subdivisions of the ventroposterior nuclear complex and the anterior pulvinar nucleus in squirrel monkeys , 1990, The Journal of comparative neurology.

[10]  P. Rakić,et al.  Heterogeneous afferents to the inferior parietal lobule of the rhesus monkey revealed by the retrograde transport method , 1977, Brain Research.

[11]  L. Benevento,et al.  The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (macaca mulatta): An autoradiographic study , 1976, Brain Research.

[12]  L A Krubitzer,et al.  The somatosensory thalamus of monkeys: Cortical connections and a redefinition of nuclei in marmosets , 1992, The Journal of comparative neurology.

[13]  Leslie G. Ungerleider,et al.  Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys , 1993, The Journal of comparative neurology.

[14]  B. Connors,et al.  Efficacy of Thalamocortical and Intracortical Synaptic Connections Quanta, Innervation, and Reliability , 1999, Neuron.

[15]  F Mauguiere,et al.  Anatomical evidence for medial pulvinar connections with the posterior cingulate cortex, the retrosplenial area, and the posterior parahippocampal gyrus in monkeys , 1985, The Journal of comparative neurology.

[16]  D. B. Bender,et al.  Retinotopic organization of macaque pulvinar. , 1981, Journal of neurophysiology.

[17]  M. Goodale,et al.  Chapter 28 Visual pathways to perception and action , 1993 .

[18]  M. Goodale,et al.  Visual pathways to perception and action. , 1993, Progress in brain research.

[19]  T. Yin,et al.  Subcortical projections of the inferior parietal cortex (area 7) in the stump‐tailed monkey , 1984, The Journal of comparative neurology.

[20]  J. Kaas,et al.  Thalamic connections of the dorsomedial visual area in primates , 1998, The Journal of comparative neurology.

[21]  J. Kaas,et al.  Do superior colliculus projection zones in the inferior pulvinar project to MT in primates? , 1999, The European journal of neuroscience.

[22]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[23]  R. Weller,et al.  Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys , 1993, Visual Neuroscience.

[24]  K. Rockland Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1) , 1996, The Journal of comparative neurology.

[25]  D L Rosene,et al.  Corticothalamic connections of auditory‐related areas of the temporal lobe in the rhesus monkey , 1994, The Journal of comparative neurology.

[26]  L. Benevento,et al.  Projections of the medial pulvinar to orbital cortex and frontal eye fields in the rhesus monkey (Macaca mulatta) , 1975, Experimental Neurology.

[27]  C. Cusick,et al.  Neurochemical organization of inferior pulvinar complex in squirrel monkeys and macaques revealed by acetylcholinesterase histochemistry, calbindin and Cat‐301 immunostaining, and Wisteria floribunda agglutinin binding , 1999, The Journal of comparative neurology.

[28]  M. Mesulam,et al.  Neural inputs into the temporopolar cortex of the rhesus monkey , 1987, The Journal of comparative neurology.

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

[30]  E. Irle,et al.  Cortical and subcortical afferent connections of the primate's temporal pole: A study of rhesus monkeys, squirrel monkeys, and marmosets , 1985, The Journal of comparative neurology.

[31]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[32]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. Robinson,et al.  Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. , 1978, Journal of neurophysiology.

[34]  M E Goldberg,et al.  Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields , 1988, The Journal of comparative neurology.

[35]  J. Kaas,et al.  Prefrontal connections of the parabelt auditory cortex in macaque monkeys , 1999, Brain Research.

[36]  R. Guillery,et al.  On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  C. Cusick,et al.  Effects of chronic monocular enucleation on calcium binding proteins calbindin-D28k and parvalbumin in the lateral geniculate nucleus of adult rhesus monkeys , 1994, Brain Research.

[38]  D. Pandya,et al.  Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: A study with a new method for horseradish peroxidase histochemistry , 1977, Brain Research.

[39]  H. Read,et al.  Construction and Representation of Visual Space in the Inferior Parietal Lobule , 1997 .

[40]  J. Smeets What do fast goal-directed movements teach us about equilibrium-point control? , 1992 .

[41]  J. Trojanowski,et al.  Medial pulvinar afferents to frontal eye fields in rhesus monkey demonstrated by horseradish peroxidase. , 1974, Brain research.

[42]  D. Pandya,et al.  Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: A WGA‐HRP and fluorescent tracer study , 1990, The Journal of comparative neurology.

[43]  C. Geula,et al.  Architecture of connectivity within a cingulo-fronto-parietal neurocognitive network for directed attention. , 1993, Archives of neurology.

[44]  K. Rockland,et al.  Single axon analysis of pulvinocortical connections to several visual areas in the Macaque , 1999, The Journal of comparative neurology.

[45]  R. Andersen,et al.  The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: Divergent cortical projections from cell clusters in the medial pulvinar nucleus , 1985, The Journal of comparative neurology.

[46]  B. Seltzer,et al.  Human thalamus: neurochemical mapping of inferior pulvinar complex. , 1999, Neuroreport.

[47]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

[48]  J. T. Weber,et al.  Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr , 1993, The Journal of comparative neurology.

[49]  L. Benevento,et al.  The organization of connections between the pulvinar and visual area MT in the macaque monkey , 1983, Brain Research.

[50]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

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

[52]  S. Hsu,et al.  Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[53]  L. Benevento,et al.  A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey , 1979, Brain Research.

[54]  D. Pandya,et al.  Corticothalamic connections of extrastriate visual areas in rhesus monkeys , 2022 .

[55]  D. V. van Essen,et al.  A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  D. Pandya,et al.  Thalamic connections of the cortex of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[57]  Leslie G. Ungerleider,et al.  Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey , 1983, The Journal of comparative neurology.

[58]  E. Salzmann Attention and memory trials during neuronal recording from the primate pulvinar and posterior parietal cortex (area PG) , 1995, Behavioural Brain Research.

[59]  J. Kaas,et al.  The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex , 1979, The Journal of comparative neurology.

[60]  M M Mesulam,et al.  Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus , 1984, The Journal of comparative neurology.

[61]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[62]  B. Seltzer,et al.  Overlapping and nonoverlapping cortical projections to cortex of the superior temporal sulcus in the rhesus monkey: Double anterograde tracer studies , 1996 .

[63]  R. Andersen,et al.  Callosal and prefrontal associational projecting cell populations in area 7A of the macaque monkey: A study using retrogradely transported fluorescent dyes , 1985, The Journal of comparative neurology.

[64]  L. Fogassi,et al.  Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  S. Petersen,et al.  The pulvinar and visual salience , 1992, Trends in Neurosciences.

[66]  L. Benevento,et al.  The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey , 1983, The Journal of comparative neurology.

[67]  R. Gattass,et al.  Visuotopic organization of the Cebus pulvinar: A double representation of the contralateral hemifield , 1978, Brain Research.

[68]  D. Pandya,et al.  Corticothalamic connections of the posterior parietal cortex in the rhesus monkey , 1985, The Journal of comparative neurology.

[69]  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.

[70]  E. G. Jones,et al.  Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[72]  Leslie G. Ungerleider,et al.  Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys , 1993, Visual Neuroscience.

[73]  D. LaBerge,et al.  Positron emission tomographic measurements of pulvinar activity during an attention task , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[75]  E. G. Jones,et al.  Differential thalamic relationships of sensory‐motor and parietal cortical fields in monkeys , 1979, The Journal of comparative neurology.

[76]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[77]  R. L. Crouch Nuclear Configuration of Thalamus of Macacus Rhesus , 1933 .

[78]  V. Mountcastle,et al.  Parietal lobe mechanisms for directed visual attention. , 1977, Journal of neurophysiology.

[79]  J. Lynch,et al.  The spatial distribution of pulvinar neurons that project to two subregions of the inferior parietal lobule in the macaque. , 1992, Cerebral cortex.

[80]  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.

[81]  Leslie G. Ungerleider,et al.  Subcortical projections of area MT in the macaque , 1984, The Journal of comparative neurology.

[82]  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.

[83]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[84]  Leslie G. Ungerleider,et al.  Subcortical connections of visual areas MST and FST in macaques , 1992, Visual Neuroscience.

[85]  D. Pandya,et al.  Anatomy of the auditory cortex. , 1995, Revue neurologique.

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

[87]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[88]  Margaret T. T. Wong-Riley,et al.  Connections between the pulvinar nucleus and the prestriate cortex in the squirrel monkey as revealed by peroxidase histochemistry and autoradiography , 1977, Brain Research.

[89]  J. Trojanowski,et al.  Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey , 1976, The Journal of comparative neurology.

[90]  David P. Friedman,et al.  Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque , 1986, The Journal of comparative neurology.

[91]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[92]  C. Cusick,et al.  Neurochemical subdivisions of the inferior pulvinar in macaque monkeys , 1995, The Journal of comparative neurology.

[93]  D. Pandya,et al.  Corticostriatal connections of extrastriate visual areas in rhesus monkeys , 1997, The Journal of comparative neurology.

[94]  A. Morel,et al.  Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey , 1992, Visual Neuroscience.

[95]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[96]  A. Hendrickson,et al.  The morphology and distribution of striate cortex terminals in the inferior and lateral subdivision of the Macaca monkey pulvinar , 1979, The Journal of comparative neurology.

[97]  H. Burton,et al.  The posterior thalamic region and its cortical projection in new world and old world monkeys , 1976, The Journal of comparative neurology.

[98]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

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

[100]  S. Petersen,et al.  Contributions of the pulvinar to visual spatial attention , 1987, Neuropsychologia.

[101]  M Steriade,et al.  Leading role of thalamic over cortical neurons during postinhibitory rebound excitation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[102]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

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

[104]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[105]  C. Cusick,et al.  Area V1 in macaque monkeys projects to multiple histochemically defined subdivisions of the inferior pulvinar complex , 1997, Brain Research.

[106]  E. G. Jones,et al.  A projection from the medial pulvinar to the amygdala in primates , 1976, Brain Research.

[107]  J. Kaas,et al.  Architectonic subdivisions of the inferior pulvinar in New World and Old World monkeys , 1997, Visual Neuroscience.

[108]  L. Benevento,et al.  Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey , 1995, Visual Neuroscience.

[109]  H. Kennedy,et al.  A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[110]  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.

[111]  J. Kaas,et al.  Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys , 1985, The Journal of comparative neurology.

[112]  L. Benevento,et al.  Histochemical and architectonic differentiation of zones of pretectal and collicular inputs to the pulvinar and dorsal lateral geniculate nuclei in the macaque , 1986, The Journal of comparative neurology.

[113]  N Dürmüller,et al.  Role of Thalamic and Cortical Neurons in Augmenting Responses and Self-Sustained Activity: Dual Intracellular Recordings In Vivo , 1998, The Journal of Neuroscience.

[114]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[115]  V. Casagrande A third parallel visual pathway to primate area V1 , 1994, Trends in Neurosciences.

[116]  Finn A. GENnS Distribution of Acetyl Cholinesterase in the Hippocampal Region of the Guinea Pig , 1972 .