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Sensorimotor unit activity related to intention in the Pulvinar of behaving Cebus Apella monkeys

Summary

Previous observations made in our laboratory in a waking behaving Cebus Apella monkey revealed that neurons of the Pulvinar nucleus of the thalamus discharged preferentially in relation to intentional movements of the limbs and eyes. We give here a description of further observations made in two waking, behaving Cebus Apella monkeys trained to perform two tasks: in the first to make saccadic eye movements to eccentrically placed visual targets; in the second, to make projection movements of the arm and hand to touch targets within arm's reach. The electrical activity of thalamic neurons was recorded extracellularly and records were made simultaneously of the horizontal eye movements and of tasks events.

Four-hundred-sixty-five neurons were studied: of these, the activity of 272 could be correlated with behavioral events, while the remaining 193 could not be correlated or classified in this manner. The cells identified were classed in five groups, as follows: (1) neurons active during attentive fixation of a target, but which did not respond to our ordinary visual test stimuli; (2) neurons active during projection movements of the arm or manipulation with the hand, but which were not active during casual movements of the hand or arm, and which were not activated by passive somatic sensory stimuli; (3) those active before, during or after evoked saccadic movements of the eyes, but which were not activated by our testing visual stimuli; (4) neurons active during tracking movements of the eyes, or during projection movements of the arm, alone, but which discharged maximally when these two events occurred simultaneously; and, (5) neurons active during both saccadic movements of the eyes and during projection movements of the arm. We regularly observed, for each of these classes of neurons of the Pulvinar, that optimal correlated activity depended upon the intentional nature of the associated behavioral events, and the animal's attention to them.

We conclude that there exists at the level of the Pulvinar a neural correlate of certain evolving behavioral events, and particularly of intentional activity such as the projection of the arm or the direction of gaze towards targets of interest in the immediately surrounding visual environment. The regions of the Pulvinar containing neurons with these properties are reciprocally related to association areas of the Neocortex known to contain neurons with similar properties. It can then be concluded from both anatomical and electrophysiological observations that the Pulvinar is an essential part of the system controlling these complex behavioral events.

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References

  • Acuña C, González F, Domínguez R (1981) Actividad unitaria extraneuronal en el pulvinar de monos durante la realización de una tarea de conducta. FESBE-2 (Madrid) 12: 23

    Google Scholar 

  • Acuña C, González F, Domínguez R (1982a) Sensorimotor interaction in the pulvinar of behaving monkeys. Neuroscience 7: S2

    Google Scholar 

  • Acuña C, González F, Domínguez R (1982b) Pulvinar unit activity related with intentional behavior in behaving monkeys (Cebus Apella). Neurosci Lett [Suppl] 10: S34

    Google Scholar 

  • Armstrong E (1981) A quantitative comparison of the Hominoid thalamus-IV posterior association nuclei.The pulvinar and lateral posterior nucleus. Am J Phys Anthropol 55: 369–383

    Google Scholar 

  • Bender DB (1981) Retinotopic organization of macaque pulvinar. J Neurophysiol 3: 672–693

    Google Scholar 

  • Bender DB (1982) Receptive-field properties of neurons in the macaque inferior pulvinar. J Neurophysiol 48: 1–17

    Google Scholar 

  • Benevento LA, Fallon JH (1975) The ascending projections of the superior colliculus in the rhesus monkey (Macaca Mulatta). J Comp Neurol 160: 339–362

    Google Scholar 

  • Benevento LA, Rezak M (1976) The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca Mulatta): An autoradiographic study. Brain Res 108: 1–24

    Google Scholar 

  • Benevento LA, Rezak M, Santos-Anderson R (1977a) An autoradiographic study of the projections of the pretectum in the rhesus monkey (Macaca Mulatta): Evidence for sensorimotor links to the thalamus and oculomotor nuclei. Brain Res 127: 197–218

    Google Scholar 

  • Benevento LA, Davis B (1977b) Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: An autoradiographic study. Exp Brain Res 30: 405–424

    Google Scholar 

  • Benevento LA, Miller J (1981) Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey. J Neurosci 11: 1268–1278

    Google Scholar 

  • Berson DM, Graybiel AM (1978) Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent connections. Brain Res 147: 139–148

    Google Scholar 

  • Bizzi E (1968) Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp Brain Res 6: 69–80

    Google Scholar 

  • Bizzi E, Schiller PM (1970) Single unit activity in the frontal eye fields of unanesthetized monkeys during eye and head movements. Exp Brain Res 10: 151–159

    Google Scholar 

  • Caminiti R, Kalaska JF, Massey JT, Georgopoulus AP (1982) Cerebral cortical mechanisms related to spatial coding of movement. Neuroscience [Suppl] 7: S35

    Google Scholar 

  • Campos-Ortega JA, Hayhow WR (1972) On the organization of the visual cortical projection to the pulvinar in macaca mulatta. Brain Behav Evol 6: 394–423

    Google Scholar 

  • Cooper IS, Amin I, Chandra R, Waltz JM (1974) Clinical physiology of motor contributions of the pulvinar in man: A study of cryopulvinectomy. In: Cooper et al. (eds) The Pulvinar-LP complex. Thomas, Springfield, pp 200–232

    Google Scholar 

  • Crighel E, Kreindler A (1976) Relations between the pulvinar lateralis posterior complex and the neural systems involved in the organization of the motor pattern. Acta Physiol Acad Sci Hung 48: 399–406

    Google Scholar 

  • Crighel E (1978) The role of the pulvinar-lateralis posterior complex of the thalamus in the organization of motor patterns. In: Lissak K (ed) Neural and neurohormonal organization of motivated behavior. Akad Kiado, Budapest, pp 65–82

    Google Scholar 

  • Crommelinck M, Roucoux A, Meulders M (1977) Eye movements evoked by stimulation of lateral posterior nucleus and pulvinar in the alert cat. Brain Res 124: 361–366

    Google Scholar 

  • Chalupa LM, Coyle RS, Lindsley DB (1976) Effect of pulvinar lesions on visual pattern discrimination in monkeys. J Neurophysiol 39: 354–369

    Google Scholar 

  • Chalupa LM (1977) A review of cat and monkey studies implicating the pulvinar in visual functions. Behav Biol 20: 149–167

    Google Scholar 

  • Chow KL (1950) A retrograde cell degeneration study of the cortical projections field of the pulvinar in the monkey. J Comp Neurol 93: 313–340

    Google Scholar 

  • Chow KL (1954) Lack of behavioral effects following destruction of some thalamic association nuclei in monkey. Arch Neurol Psychiatry 71: 762–771

    Google Scholar 

  • Fujii M, Yoshii N (1979) Hypothalamic projecton to the pulvinar-LP complex in the cat: A study by the silver impregnation method. Neurosci Lett 12: 247–252

    Google Scholar 

  • Gattass R, Oswaldo-Cruz E, Sousa APB (1978a) Visuotopic organization of the cebus pulvinar: A double representation of the contralateral hemifield. Brain Res 152: 1–16

    Google Scholar 

  • Gattass R, Sousa APB, Oswaldo-Cruz E (1978b) Singe unit response types in the pulvinar of the cebus monkey to multisensory stimulation. Brain Res 158: 75–87

    Google Scholar 

  • Gattass R, Owsaldo-Cruz E, Sousa APB (1979) Visual receptive fields of units in the pulvinar of cebus monkey. Brain Res 160: 413–430

    Google Scholar 

  • Goldberg ME, Wurtz RH (1972) Activity of superior colliculus in behaving monkey. I. Visual receptive field of single neurons. J Neurophysiol 35: 542–559

    Google Scholar 

  • Goldberg ME, Bushnell MC (1981) Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields spacifically related to saccades. J Neurophysiol 46: 773–787

    Google Scholar 

  • Graham J (1982) Some topographical connections of the striate cortex with subcortical structures in macaca fascicularis. Exp Brain Res 47: 1–14

    Google Scholar 

  • Harting JK, Hall WC, Diamond IJ (1972) Evolution of the pulvinar. Brain Behav Evol 6: 424–452

    Google Scholar 

  • Huang ChC, Lindsley DB (1973) Polisensory responses and sensory interaction in pulvinar and related postero-lateral thalamic nuclei in cat. Electroencephalogr Clin Neurol 34: 265–280

    Google Scholar 

  • Hyvärinen J (1982) Posterior parietal lobe of the primate brain. Physiol Rev 62: 1060–1129

    Google Scholar 

  • Ingvar S (1923) On thalamic evolution. Acta Med Scand 59: 696–709

    Google Scholar 

  • Itoh K, Mizuno N, Sugimoto T, Nomura S, Nakamura Y, Konishi A (1979) A cerebelo-pulvino-cortical and a retino-pulvinocortical pathways in the cat as revealed by the use of the anterograde and retrograde transport of horseradish peroxidase. J Comp Neurol 187: 349–358

    Google Scholar 

  • Kievit J, Kuypers HGJ (1977) Organization of the thalamocortical connexions to the frontal lobe in the rhesus monkey. Exp Brain Res 29: 299–322

    Google Scholar 

  • Keys W, Robinson DL (1979) Eye movement dependent enhancement of visual responses in the pulvinar nucleus of the monkey. Soc Neurosci Abstr 5: 791

    Google Scholar 

  • Lin CS, Kaas JH (1979) The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from superior colliculus and subdivisions of visual cortex. J Comp Neurol 187: 655–578

    Google Scholar 

  • Lin CS, Kaas JH (1980) Projections from the medial nucleus of the inferior pulvinar complex to the middle temporal area of the visual cortex. Neuroscience 5: 2219–2228

    Google Scholar 

  • Lynch JC, Mountcastle VB, Talbot WH, Yin TCT (1977) Parietal lobe mechanisms for directed visual attention. J Neurophysiol 40: 362–389

    Google Scholar 

  • Lynch JC (1980) The functional organization of posterior parietal association cortex. Behav Brain Sci 3: 485–534

    Google Scholar 

  • Manocha SL, Shantha TR, Bourne GH (1968) A stereotaxic atlas of the brain of the cebus monkey (Cebus Apella). Oxford University Press, Oxford

    Google Scholar 

  • Martin-Rodriguez JG, Buño W, Garcia-Austt E (1982) Human pulvinar units spontaneous activity and sensory-motor influences. Electroenceph Clin Neurophysiol 54: 388–398

    Google Scholar 

  • Mathers LH, Rapsardi SC (1973) Visual and somatosensory receptive fields of neurons in the squirrel monkey pulvinar. Brain Res 64: 65–83

    Google Scholar 

  • Mauguiere F, Baleydier C (1978) Topographical organization of medial pulvinar neurons sending fibres to Brodman's areas 7, 21 and 22 in the monkey. Exp Brain Res 31: 605–607

    Google Scholar 

  • Mohler CW, Goldberg ME, Wurtz RH (1973) Visual receptive fields of frontal eye field neurons. Brain Res 61: 385–389

    Google Scholar 

  • Mountcastle VB, Lynch JC, Georgopoulus A, Sakata H, Acuña C (1975) Posterior parietal association cortex of the monkey: Command functions for operations within extrapersonal space. J Neurophysiol 37: 871–908

    Google Scholar 

  • Ogren M, Hendrickson A (1976) Pathways between striate cortex and subcortical regions in Macaca Mulatta and saimiri sciureus: Evidence for a reciprocal pulvinar connections. Exp Neurol 53: 780–800

    Google Scholar 

  • Ogren MP, Hendrickson AE (1977) The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey. Brain Res 137: 343–350

    Google Scholar 

  • Palestini M, Modes E, Infante C, Saavedra H (1977) Electrophysiological relationships between the caudate nucleus and the pulvinar-lateralis posterior complex. Arch Ital Biol 115: 185–198

    Google Scholar 

  • Pearson RCA, Brodal P, Powell TPS (1978) The projection of the thalamus upon the parietal lobe in the monkey. Brain Res 144: 143–148

    Google Scholar 

  • Perryman KM, Lindsley DF, Lindsley DB (1980) Pulvinar neuron responses to spontaneous and trained eye movements and to light flashes in squirrel monkeys. Electroencephalogr Clin Neurol 49: 152–161

    Google Scholar 

  • Porrino LJ, Crane AM, Goldman-Rakic PS (1981) Direct and indirect pathways from the amygdala to the frontal lobe in Rhesus monkey. J Comp Neurol 198: 121–136

    Google Scholar 

  • Rezak M, Benevento LA (1979) 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. Brain Res 167: 19–40

    Google Scholar 

  • Richardson DE, Zorub DS (1970) Sensory function of the pulvinar. Confin Neurol 32: 165–173

    Google Scholar 

  • Robinson DL, Keys W (1981) Visuomotor properties of neurons in superior colliculus and pulvinar nucleus of the monkey. In: Szentagothai J, Tamori J, Plakoviti M (eds) Advances in Physiological Sciences, vol 2. Regulatory functions of the CNS subsystems. Pergamon Press, Oxford New York, pp 279–285

    Google Scholar 

  • Sakata H, Shibutani H, Kawano K (1980) Spatial properties of visual fixation neurons in posterior parietal association cortex of the monkey. J Neurophysiol 43: 1654–1672

    Google Scholar 

  • Schott B, Laurent B, Mauguiere F, Chazot G (1981) Négligence motrice par hematome thalamique droit. Rev Neurol (Paris) 137: 447–455

    Google Scholar 

  • Siquiera EB (1971) The cortical connections of the nucleus pulvinaris of the dorsal thalamus in the rhesus monkey. Int J Neurol 8: 139–154

    Google Scholar 

  • Spreafico R, Kirk C, Franceschetti S, Avanzini G (1980) Brain stem projections to the pulvinar-lateralis posterior complex of the cat. Exp Brain Res 40: 209–220

    Google Scholar 

  • Tekian A, Afiki AK (1981) Efferent connections of the pulvinar nucleus in the cat. J Anat 132: 249–265

    Google Scholar 

  • Trojanowski JQ, Jacobson S (1974) Medial pulvinar afferents to frontal eye fields in rhesus monkey demonstrated by horseradish peroxidase. Brain Res 80: 395–411

    Google Scholar 

  • Trojanowski JQ, Jacobson S (1975) Peroxidase labeled subcortical afferents to pulvinar in rhesus monkey. Brain Res 97: 144–150

    Google Scholar 

  • Trojanowski JQ, Jacobson S (1976) Area and laminar distribution of some pulvinar cortical efferents in rhesus monkeys. J Comp Neurol 169: 371–391

    Google Scholar 

  • Ungerleider LD, Christensen CA (1977) Pulvinar lesions in monkeys produced abnormal eye movements during visual discrimination training. Brain Res 136: 189–196

    Google Scholar 

  • Ungerleider LH, Christensen CA (1979) Pulvinar lesions in monkeys produce abnormal scanning of a complex visual array. Neuropsychologia 17: 493–501

    Google Scholar 

  • Walker AE (1938) The primate thalamus. Chicago University Press, Chicago

    Google Scholar 

  • Wei JY, Marczynski TJ (1979) Pulvinar and lateral geniculate neuronal activity in the cat during operantly conditioned appetitive behavior. Brain Res 166: 9–25

    Google Scholar 

  • Whitsel BL, Rustioni A, Dreyer DA, Loe PR, Allen EE, Metz CB (1978) Thalamic projections to S-I in macaque monkey. J Comp Neurol 178: 385–409

    Google Scholar 

  • Wurtz RH, Mohler CW (1976) Organization of monkey superior colliculus: Enhanced visual response of superficial layer cells. J Neurophysiol 39: 745–765

    Google Scholar 

  • Yoshii N, Fuji M, Mizokami T (1978) Hypothalamic projection to the pulvinar-LP complex in the cat: A study by the HRP method. Brain Res 155: 343–346

    Google Scholar 

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This work was partially supported by aids from FISS 64/81, and the Comisión Asesora de Investigatión Científica y Técnica 735/ 82, Spain

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Acuña, C., Gonzalez, F. & Dominguez, R. Sensorimotor unit activity related to intention in the Pulvinar of behaving Cebus Apella monkeys. Exp Brain Res 52, 411–422 (1983). https://doi.org/10.1007/BF00238034

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Key words

  • Pulvinar
  • Behaving monkeys
  • Extracellular unit activity