Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells

Science

Volumn 278, Issue 5337, 1997, Pages 463-467

  Chen, Wei R ^a   Midtgaard, Jens ^b   Shepherd, Gordon M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DENDRITE; MITRAL CELL; NERVE CONDUCTION; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM;

ACTION POTENTIALS; ANIMALS; DENDRITES; ELECTRIC STIMULATION; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; OLFACTORY BULB; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

ANIMALIA; MAMMALIA;

EID: 0030668381     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.278.5337.463     Document Type: Article

References (40)

1. S. Ramon y Cajal, Histologie du Système Nerveux de l'Homme et des Vertébrés (Maloine, Paris, 1911); G. M. Shepherd, in Handbook of Physiology, Section 1: The Nervous System, E. R. Kandel, Ed. (American Physiological Society: Bethesda, MD, 1977), vol. 1, part 2, pp. 945-968; J. W. Scott and T. A. Harrison, in Neurobiology of Taste and Smell, T. E. Finger and W. L. Silver, Eds. (Wiley, New York, 1987), pp. 151-178; K. Mori, Prog. Neurobiol. 29, 275 (1987).
2. S. Ramon y Cajal, Histologie du Système Nerveux de l'Homme et des Vertébrés (Maloine, Paris, 1911); G. M. Shepherd, in Handbook of Physiology, Section 1: The Nervous System, E. R. Kandel, Ed. (American Physiological Society: Bethesda, MD, 1977), vol. 1, part 2, pp. 945-968; J. W. Scott and T. A. Harrison, in Neurobiology of Taste and Smell, T. E. Finger and W. L. Silver, Eds. (Wiley, New York, 1987), pp. 151-178; K. Mori, Prog. Neurobiol. 29, 275 (1987).
3. S. Ramon y Cajal, Histologie du Système Nerveux de l'Homme et des Vertébrés (Maloine, Paris, 1911); G. M. Shepherd, in Handbook of Physiology, Section 1: The Nervous System, E. R. Kandel, Ed. (American Physiological Society: Bethesda, MD, 1977), vol. 1, part 2, pp. 945-968; J. W. Scott and T. A. Harrison, in Neurobiology of Taste and Smell, T. E. Finger and W. L. Silver, Eds. (Wiley, New York, 1987), pp. 151-178; K. Mori, Prog. Neurobiol. 29, 275 (1987).
4. S. Ramon y Cajal, Histologie du Système Nerveux de l'Homme et des Vertébrés (Maloine, Paris, 1911); G. M. Shepherd, in Handbook of Physiology, Section 1: The Nervous System, E. R. Kandel, Ed. (American Physiological Society: Bethesda, MD, 1977), vol. 1, part 2, pp. 945-968; J. W. Scott and T. A. Harrison, in Neurobiology of Taste and Smell, T. E. Finger and W. L. Silver, Eds. (Wiley, New York, 1987), pp. 151-178; K. Mori, Prog. Neurobiol. 29, 275 (1987).
5. W. Rall, G. M. Shepherd, T. S. Reese, M. W. Brightman, Exp. Neurol. 14, 44 (1966); W. Rall and G. M. Shepherd, J. Neurophysiol. 31, 884 (1968); C. E. Jahr and R. A. Nicoll, J. Physiol. (London) 326, 213 (1982).
6. W. Rall, G. M. Shepherd, T. S. Reese, M. W. Brightman, Exp. Neurol. 14, 44 (1966); W. Rall and G. M. Shepherd, J. Neurophysiol. 31, 884 (1968); C. E. Jahr and R. A. Nicoll, J. Physiol. (London) 326, 213 (1982).
7. W. Rall, G. M. Shepherd, T. S. Reese, M. W. Brightman, Exp. Neurol. 14, 44 (1966); W. Rall and G. M. Shepherd, J. Neurophysiol. 31, 884 (1968); C. E. Jahr and R. A. Nicoll, J. Physiol. (London) 326, 213 (1982).
8. G. M. Shepherd and C. A. Greer, in The Synaptic Organization of the Brain, G. M. Shepherd, Ed. (Oxford Univ. Press, New York, ed. 3, 1990), pp. 133-169.
9. - in the pipette have given similar results. The criteria for data analysis were a resting membrane potential greater than -50 mV and an overshooting somatic action potential. In some experiments, 0.1% biocytin and 0.1% lucifer yellow potassium salt were included in the pipette solution to analyze the morphology of recorded mitral cells. Recordings were made in bridge mode using an Axoclamp-2A amplifier (bandpass: DC-30 kHz). In order to achieve a fast sampling rate for two channels of membrane potential and two channels of membrane current, we employed two computer systems synchronized by an external trigger. Membrane potentials were digitized at 20 kHz with an Instrutech ITC-16 interface and a PowerMac computer. Membrane currents were recorded at 2.5 kHz with an Axon TL-1 interface and an IBM-compatible 486 computer. The positions of recording and stimulating electrodes were photographed with a Scion LG-3 frame grabber, and the distance between the somatic and dendritic recording sites was measured on the computer. To stimulate the olfactory nerve, a concentric bipolar electrode (tip diameter of 25 μm) was placed in the olfactory nerve layer just above the glomerulus to which the recorded mitral cell projected its primary dendrite. Another stimulating electrode was located laterally in the deep EPL to elicit inhibitory synaptic input to the secondary dendrites of the recorded mitral cell. This electrode was generally 300 to 800 μm from the recorded mitral cell primary dendrite. The stimulating electrodes were connected to two electronic isolators and constant current stimuli of variable strength (10 μA to 2 mA) were delivered.
10. W. T. Nickell, M. T. Shipley, M. M. Behbehani, Brain Res. Bull. 39, 57 (1996); M. Ennis, L. A. Zimmer, M. T. Shipley, Neuroreport 7, 989 (1996); G. J. Stuart, H.-U. Dodt, B. Sakmann, Pfleugers Arch. Eur. J. Physiol. 423, 511 (1993).
11. W. T. Nickell, M. T. Shipley, M. M. Behbehani, Brain Res. Bull. 39, 57 (1996); M. Ennis, L. A. Zimmer, M. T. Shipley, Neuroreport 7, 989 (1996); G. J. Stuart, H.-U. Dodt, B. Sakmann, Pfleugers Arch. Eur. J. Physiol. 423, 511 (1993).
12. W. T. Nickell, M. T. Shipley, M. M. Behbehani, Brain Res. Bull. 39, 57 (1996); M. Ennis, L. A. Zimmer, M. T. Shipley, Neuroreport 7, 989 (1996); G. J. Stuart, H.-U. Dodt, B. Sakmann, Pfleugers Arch. Eur. J. Physiol. 423, 511 (1993).
13. W. R. Chen and G. M. Shepherd, Brain Res. 745, 189 (1997).
14. D. B. Jaffe et al., Nature 357, 244 (1992); G. J. Stuart and B. Sakmann, ibid. 367, 69 (1994); N. Spruston, Y. Schiller, G. Stuart, B. Sakmann, Science 268, 297 (1995); K. Svoboda, W. Denk, D. Kleinfeld, D. W. Tank, Nature 385, 161 (1997); J. C. Magee and D. A. Johnston, Science 275, 209 (1997).
15. D. B. Jaffe et al., Nature 357, 244 (1992); G. J. Stuart and B. Sakmann, ibid. 367, 69 (1994); N. Spruston, Y. Schiller, G. Stuart, B. Sakmann, Science 268, 297 (1995); K. Svoboda, W. Denk, D. Kleinfeld, D. W. Tank, Nature 385, 161 (1997); J. C. Magee and D. A. Johnston, Science 275, 209 (1997).
16. D. B. Jaffe et al., Nature 357, 244 (1992); G. J. Stuart and B. Sakmann, ibid. 367, 69 (1994); N. Spruston, Y. Schiller, G. Stuart, B. Sakmann, Science 268, 297 (1995); K. Svoboda, W. Denk, D. Kleinfeld, D. W. Tank, Nature 385, 161 (1997); J. C. Magee and D. A. Johnston, Science 275, 209 (1997).
17. D. B. Jaffe et al., Nature 357, 244 (1992); G. J. Stuart and B. Sakmann, ibid. 367, 69 (1994); N. Spruston, Y. Schiller, G. Stuart, B. Sakmann, Science 268, 297 (1995); K. Svoboda, W. Denk, D. Kleinfeld, D. W. Tank, Nature 385, 161 (1997); J. C. Magee and D. A. Johnston, Science 275, 209 (1997).
18. D. B. Jaffe et al., Nature 357, 244 (1992); G. J. Stuart and B. Sakmann, ibid. 367, 69 (1994); N. Spruston, Y. Schiller, G. Stuart, B. Sakmann, Science 268, 297 (1995); K. Svoboda, W. Denk, D. Kleinfeld, D. W. Tank, Nature 385, 161 (1997); J. C. Magee and D. A. Johnston, Science 275, 209 (1997).
19. W. R. Chen, J. Midtgaard, G. M. Shepherd, data not shown.
20. J. Leveteau and P. MacLeod, Science 175, 170 (1965); J. S. Kauer, J. Physiol. (London) 243, 695 (1975); D. P. Wellis and J. W. Scott, Chem. Senses 12, 707 (1987); K. A. Hamilton and J. S. Kauer, Brain Res. 338, 181 (1989).
21. J. Leveteau and P. MacLeod, Science 175, 170 (1965); J. S. Kauer, J. Physiol. (London) 243, 695 (1975); D. P. Wellis and J. W. Scott, Chem. Senses 12, 707 (1987); K. A. Hamilton and J. S. Kauer, Brain Res. 338, 181 (1989).
22. J. Leveteau and P. MacLeod, Science 175, 170 (1965); J. S. Kauer, J. Physiol. (London) 243, 695 (1975); D. P. Wellis and J. W. Scott, Chem. Senses 12, 707 (1987); K. A. Hamilton and J. S. Kauer, Brain Res. 338, 181 (1989).
23. J. Leveteau and P. MacLeod, Science 175, 170 (1965); J. S. Kauer, J. Physiol. (London) 243, 695 (1975); D. P. Wellis and J. W. Scott, Chem. Senses 12, 707 (1987); K. A. Hamilton and J. S. Kauer, Brain Res. 338, 181 (1989).
24. M. Hausser, G. Stuart, C. Racca, B. Sakmann, Neuron 15, 637 (1995).
25. W. A. Spencer and E. R. Kandel, J. Neurophysiol. 24, 272 (1961).
26. K. Mori, M. C. Nowycky, G. M. Shepherd, J. Neurosci. 2, 497 (1982); K. Mori and S. F. Takagi, Brain Res. 100, 685 (1975).
27. K. Mori, M. C. Nowycky, G. M. Shepherd, J. Neurosci. 2, 497 (1982); K. Mori and S. F. Takagi, Brain Res. 100, 685 (1975).
28. H.-T. Chang, Cold Spring Harbor Symp. Quant. Biol. 17, 189 (1952); B. G. Cragg and L. H. Hamlyn, J. Physiol. (London) 129, 608 (1955); L. S. Benardo, L. M. Masukawa, D. A. Prince, J. Neurosci. 2, 1614 (1982); J. R. Huguenard, O. P. Hamill, D. A. Prince, Proc. Natl. Acad. Sci. U.S.A. 86, 2473 (1989); O. Herreras, J. Neurophysiol. 64, 1429 (1990); R. W. Turner, D. E. R. Meyers, T. L. Richardson, J. L. Barker, J. Neurosci. 11, 2270 (1991).
29. H.-T. Chang, Cold Spring Harbor Symp. Quant. Biol. 17, 189 (1952); B. G. Cragg and L. H. Hamlyn, J. Physiol. (London) 129, 608 (1955); L. S. Benardo, L. M. Masukawa, D. A. Prince, J. Neurosci. 2, 1614 (1982); J. R. Huguenard, O. P. Hamill, D. A. Prince, Proc. Natl. Acad. Sci. U.S.A. 86, 2473 (1989); O. Herreras, J. Neurophysiol. 64, 1429 (1990); R. W. Turner, D. E. R. Meyers, T. L. Richardson, J. L. Barker, J. Neurosci. 11, 2270 (1991).
30. H.-T. Chang, Cold Spring Harbor Symp. Quant. Biol. 17, 189 (1952); B. G. Cragg and L. H. Hamlyn, J. Physiol. (London) 129, 608 (1955); L. S. Benardo, L. M. Masukawa, D. A. Prince, J. Neurosci. 2, 1614 (1982); J. R. Huguenard, O. P. Hamill, D. A. Prince, Proc. Natl. Acad. Sci. U.S.A. 86, 2473 (1989); O. Herreras, J. Neurophysiol. 64, 1429 (1990); R. W. Turner, D. E. R. Meyers, T. L. Richardson, J. L. Barker, J. Neurosci. 11, 2270 (1991).
31. H.-T. Chang, Cold Spring Harbor Symp. Quant. Biol. 17, 189 (1952); B. G. Cragg and L. H. Hamlyn, J. Physiol. (London) 129, 608 (1955); L. S. Benardo, L. M. Masukawa, D. A. Prince, J. Neurosci. 2, 1614 (1982); J. R. Huguenard, O. P. Hamill, D. A. Prince, Proc. Natl. Acad. Sci. U.S.A. 86, 2473 (1989); O. Herreras, J. Neurophysiol. 64, 1429 (1990); R. W. Turner, D. E. R. Meyers, T. L. Richardson, J. L. Barker, J. Neurosci. 11, 2270 (1991).
32. H.-T. Chang, Cold Spring Harbor Symp. Quant. Biol. 17, 189 (1952); B. G. Cragg and L. H. Hamlyn, J. Physiol. (London) 129, 608 (1955); L. S. Benardo, L. M. Masukawa, D. A. Prince, J. Neurosci. 2, 1614 (1982); J. R. Huguenard, O. P. Hamill, D. A. Prince, Proc. Natl. Acad. Sci. U.S.A. 86, 2473 (1989); O. Herreras, J. Neurophysiol. 64, 1429 (1990); R. W. Turner, D. E. R. Meyers, T. L. Richardson, J. L. Barker, J. Neurosci. 11, 2270 (1991).
33. H.-T. Chang, Cold Spring Harbor Symp. Quant. Biol. 17, 189 (1952); B. G. Cragg and L. H. Hamlyn, J. Physiol. (London) 129, 608 (1955); L. S. Benardo, L. M. Masukawa, D. A. Prince, J. Neurosci. 2, 1614 (1982); J. R. Huguenard, O. P. Hamill, D. A. Prince, Proc. Natl. Acad. Sci. U.S.A. 86, 2473 (1989); O. Herreras, J. Neurophysiol. 64, 1429 (1990); R. W. Turner, D. E. R. Meyers, T. L. Richardson, J. L. Barker, J. Neurosci. 11, 2270 (1991).
34. W. G. Regehr and C. M. Armstrong, Curr. Biol. 4, 436 (1994).
35. G. Stuart, N. Spruston, B. Sakmann, M. Häusser, Trends Neurosci. 20, 125 (1997).
36. J. DeFelipe and I. Farinas, Prog. Neurobiol. 39, 563 (1992).
37. Z. F. Mainen, J. Joerges, J. R. Huguenard, T. J. Sejnowski, Neuron 15, 1427 (1995).
38. J. C. Callaway, N. Lasser-Ross, W. N. Ross, J. Neurosci. 15, 2777 (1995); H. Tsubokawa and W. N. Ross, J. Neurophysiol. 76, 2896 (1996).
39. J. C. Callaway, N. Lasser-Ross, W. N. Ross, J. Neurosci. 15, 2777 (1995); H. Tsubokawa and W. N. Ross, J. Neurophysiol. 76, 2896 (1996).
40. This work was supported by grants from the National Institute on Deafness and Other Communication Disorders (NIDCD) and by the National Institute of Mental Health, NASA, and NIDCD under the Human Brain Project (G.M.S.), and by grants from the Carlsberg Foundation, the Danish Medical Research Council, the Faculty of Health Sciences (Copenhagen University), and the Danish Medical Association's Research Fund (J.M.).