Cingulate gyrus of the cat receives projection fibers from the thalamic region ventral to the ventral border of the ventrobasal complex
Yukihiko Yasui
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorKazuo Itoh
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorHiroto Kamiya
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorTadashi Ino
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorNoboru Mizuno
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorYukihiko Yasui
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorKazuo Itoh
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorHiroto Kamiya
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorTadashi Ino
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorNoboru Mizuno
Department of Anatomy (1st Division), Faculty of Medicine, Kyoto University, Kyoto 606, Japan
Search for more papers by this authorAbstract
Direct projections to the cingulate gyrus from the thalamic region lying just ventrally to the ventral border of the ventrobasal complex (VB) were found in the cat by two sets of experiments that used WGA-HRP (wheat germ agglutinin-horseradish peroxidase conjugate).
In the first set of experiments, WGA-HRP was injected into the thalamic region around the ventral border of the VB. When the site of injection involved the thalamic region lying ventrally to the ventral border of the VB at the levels of the caudal two thirds of the VB. The cerebral cortex in the rostral part of the cingulate gyrus ipsilateral to the WGA-HRP injection contained fine HRP-positive granules, which indicated anterograde labeling of axon terminals. These labeled presumed axon terminals were mainly distributed to the superficial part of layer I, deep part of layer II, layer IV, and the most superficial part of layer V in the cingulate cortex.
In the second set of experiments, WGA-HRP was injected into the cerebral cortex of the rostral part of the cingulate gyrus. When the site of injection involved the region of the cingulate gyrus, where presumed axon terminals had been labeled in the first set of experiments, the thalamic region just ventral to the ventral margin of the caudal two-thirds of the VB ipsilateral to the WGA-HRP injection contained neuronal cell bodies labeled retrogradely.
The results indicate that some neurons that are located in the thalamic region just ventral to the ventral border of the caudal two-thirds of the VB send their axons to the cerebral cortex in the rostral part of the cingulate gyrus.
The possible significance of the thalamocingulate projection found in the present study is discussed with relation to nociceptive behavior and function.
Literature Cited
- Albé-Fessard, S. (1972) Central pathways for noxious stimuli. In C. Hirsch and Y. Zotterman (eds): Cervical Pain. Oxford: Pergamon Press, pp. 179–193.
- Amromin, G. D., B. L. Crue, A. Felsööry, and E. M. Todd (1975) Bilateral stereotaxic cingulumotomy following thoracic rhizotomy, cervical cordotomy and thalamotomy in a patient with intractable pain: A clinicopathological study. In B. L. Crue (ed): Pain Research and Treatment. New York: Academic Press, pp. 227–241.
- Baleydier, C., and F. Mauguiere (1980) The duality of the cingulate gyrus in the monkey. Neuroanatomical study and functional hypothesis. Brain 103: 525–554.
- Boivie, J. (1979) An anatomical reinvestigation of the termination of the spinothalamic tract in the monkey. J. Comp. Neurol. 186: 343–370.
- Foltz, E. L., and L. W. White (1962) Pain “relief” by frontal cingulumotomy. J. Neurosurg. 19: 89–100.
- Hassler, R., and K. Muhs-Clement (1964) Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze. J. Hirnforsch. 6: 377–420.
- Herkenham, M. (1978) The connections of the nucleus reuniens thalami: Evidence for a direct thalamo-hippocampal pathway in the rat. J. Comp. Neurol. 177: 589–610.
- Honda, C. N., S. Mense, and E. R. Perl (1983) Neurons in ventrobasal region of cat thalamus selectively responsive to noxious mechanical stimulation. J. Neurophysiol. 49: 662–673.
- Iwahori, N., and N. Mizuno (1980) A Golgi study on the zona incerta of the mouse. Anat. Embryol. (Berl.) 161: 145–158.
- Jones, E. G., and R. Y. Leavitt (1974) Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J. Comp. Neurol. 154: 349–378.
- Kaelber, W. W. (1977) Subthalamic nociceptive stimulation in the cat: Effect of secondary lesions and rostral fiber projections. Exp. Neurol. 56: 574–597.
- Kaelber, W. W., and T. B. Smith (1979) Projections of the zona incerta in the cat with stimulation controls. Exp. Neurol. 63: 177–200.
- Kawana, E., and K. Watanabe (1981) A cytoarchitectonic study of zona incerta in the rat. J. Hirnforsch. 22: 535–541.
- Kerr, F. W. L. (1975) The ventral spinothalamic tract and other ascending systems of the ventral funiculus of the spinal cord. J. Comp. Neurol. 159: 335–356.
- Kniffki, K.-D., and K. Mizumura (1983) Response of neurons in VPL and VPL-VL region of the cat to algesic stimulation of muscle and tendon. J. Neurophysiol. 49: 649–661.
- Macchi, G., M. Bentivoglio, C. D'Atena, P. Rossini, and E. Tempesta (1977) The cortical projections of the thalamic intralaminar nuclei restudied by means of the HRP retrograde axonal transport. Neurosci. Lett. 4: 121–126.
-
Matsuoka, H.
(1986)
Topographic arrangement of the projection from the anterior thalamic nuclei to the cingulate cortex in the cat.
Neurosci. Res.
4:
62–66.
10.1016/0168-0102(86)90017-9 Google Scholar
- Mehler, W. R., M. E. Feferman, and W. J. H. Nauta (1960) Ascending axon degeneration following anterolateral cordotomy: An experimental study in the monkey. Brain 83: 718–752.
- Mesulam, M.-M. (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26: 106–117.
- Nomura, S., K. Itoh, and N. Mizuno (1980) Topographical arrangement of thalamic neurons projecting to the orbital gyrus in the cat. Exp. Neurol. 67: 601–610.
- Olszewski, J. (1952) The Thalamus of the Macaca Mulatta. An Atlas for Use With the Stereotaxic Instrument. Basel: Karger.
- Price, D. D., and R. Dubner (1977) Neurons that subserve the sensory-discriminative aspects of pain. Pain 3: 307–338.
- Ricardo, J. A. (1981) Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Res. 214: 43–60.
- Rinvik, E. (1968) A re-evaluation of the cytoarchitecture of the ventral nuclear complex of the cat's thalamus on the basis of corticothalamic connections. Brain Res. 8: 237–254.
- Robertson, R. T., and S. S. Kaitz (1981) Thalamic connections with limbic cortex. I. Thalamocortical projections. J. Comp. Neurol. 195: 501–525.
- Roger, M., and J. Cadusseau (1985) Afferents to the zona incerta in the rat: A combined retrograde and anterograde study. J. Comp. Neurol. 241: 480–492.
- Romanowski, C. A. J., I. J. Mitchell, and A. R. Crossman (1985) The organisation of the efferent projections of the zona incerta. J. Anat. (Lond.) 143: 75–95.
- Rose, J. D. (1978) Distribution and properties of diencephalic neuronal responses to genital stimulation in the female cat. Exp. Neurol. 61: 231–244.
- Rose, J. E., and C. N. Woolsey (1948) Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat. J. Comp. Neurol. 89: 279–348.
- Royce, G. J., and R. J. Mourey (1985) Efferent connections of the centromedian and parafascicular thalamic nuclei: An autoradiographic investigation. J. Comp. Neurol. 235: 277–300.
- Shammah-Lagnado, S. J., N. Negrão, and J. A. Ricardo (1985) Afferent connections of the zona incerta: A horseradish peroxidase study in the rat. Neuroscience 15: 109–134.
- Sripanidkulchai, K., and J. M. Wyss (1986) Thalamic projections to retrosplenial cortex in the rat. J. Comp. Neurol. 254: 143–165.
- Steriade, M., A. Parent, N. Ropert, and A. Kitsikis (1982) Zona incerta and lateral hypothalamic afferents to the midbrain reticular core of cat – An HRP and electrophysiological study. Brain Res. 238: 13–28.
- Streit, P., and J. C. Reubi (1977) A new and sensitive staining method for axonally transported horseradish peroxidase (HRP) in the pigeon visual system. Brain Res. 126: 530–537.
-
Taguchi, H.,
T. Masuda, and
T. Yokota
(1987)
Cardiac sympathetic afferent input onto neurons in nucleus ventralis posterolateralis in cat thalamus.
Brain Res.
436:
240–252.
10.1016/0006-8993(87)91668-4 Google Scholar
- Turnbull, I. M. (1972) Bilateral cingulumotomy combined with thalamotomy or mesencephalic tractotomy for pain. Surg. Gynecol. Obstet. 134: 958–962.
-
Uemura-Sumi, M.,
J. Osterstock, and
O. E. Millhouse
(1985)
The zona incerta: Another source of centrifugal fibers to the main olfactory bulb.
Neurosci. Lett.
53:
241–245.
10.1016/0304-3940(85)90544-0 Google Scholar
- Vogt, B. A. (1985) Cingulate cortex. In A. Peters and E. G. Jones (eds): Cerebral Cortex, Vol. 4: Association and Auditory Cortices. New York: Plenum Press, pp. 89–150.
- Vogt, B. A., D. N. Pandya, and D. L. Rosene (1987) Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents. J. Comp. Neurol. 262: 256–270.
- Vogt, B. A., D. L. Rosene, and D. N. Pandya (1979) Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the monkey. Science 204: 205–207.
- Watanabe, K., and E. Kawana (1982) The cells of origin of the incertofugal projections to the tectum, thalamus, tegmentum and spinal cord in the rat: A study using the autoradiographic and horseradish peroxidase methods. Neuroscience 7: 2389–2406.
- White, J. C., and W. H. Sweet (1969) Pain and the Neurosurgeon. Springfield: Thomas.
- Willis, W. D., D. R. Kenshalo, and R. B. Leonard (1979) The cells of origin of the primate spinothalamic tract. J. Comp. Neurol. 188: 543–574.
-
Yasui, Y.,
K. Itoh,
T. Kaneko,
T. Sugimoto, and
N. Mizuno
(1986)
Direct projections from the parvocellular part of the posteromedial ventral nucleus of the thalamus to the infralimbic cortex in the cat.
Brain Res.
368:
384–388.
10.1016/0006-8993(86)90587-1 Google Scholar
- Yasui, Y., K. Itoh, T. Sugimoto, T. Kaneko, and N. Mizuno (1987) Thalamocortical and thalamo-amygdaloid projections from the parvicellular division of the posteromedial ventral nucleus in the cat. J. Comp. Neurol. 257: 253–268.
- Yokota, T., N. Koyama, and N. Matsumoto (1985) Somatotopic distribution of trigeminal nociceptive neurons in ventrobasal complex of cat thalamus. J. Neurophysiol. 53: 1387–1400.
- Yokota, T., and N. Matsumoto (1983a) Somatotopic distribution of trigeminal nociceptive specific neurons within the caudal somatosensory thalamus of cat. Neurosci. Lett. 39: 125–130.
- Yokota, T., and N. Matsumoto (1983b) Location and functional organization of trigeminal wide dynamic range neurons within the nucleus ventralis posteromedialis of the cat. Neurosci. Lett. 39: 231–236.
- Yokota, T., Y. Nishikawa, and N. Koyama (1986) Tooth pulp input to the shell region of nucleus ventralis posteromedialis of the cat thalamus. J. Neurophysiol. 56: 80–98.