Bistability of cerebellar Purkinje cells modulated by sensory stimulation

Nature Neuroscience

Volumn 8, Issue 2, 2005, Pages 202-211

  Loewenstein, Yonatan ^a,b   Mahon, Séverine ^c   Chadderton, Paul ^c   Kitamura, Kazuo ^c   Sompolinsky, Haim ^a   Yarom, Yosef ^a   Hausser, Michael ^c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOPHYSICS; CEREBELLUM CORTEX; CLIMBING FIBER; GUINEA PIG; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; RAT STRAIN; SENSORY STIMULATION; SPIKE; STIMULUS RESPONSE; TIME;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; ANIMALS, NEWBORN; CEREBELLAR CORTEX; ELECTRIC STIMULATION; EVOKED POTENTIALS; FUNCTIONAL LATERALITY; GUINEA PIGS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; PURKINJE CELLS; RATS; SYNAPSES; TIME FACTORS; VIBRISSAE;

EID: 13244249793     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1393     Document Type: Article

References (48)

1. Fuster, J.M. Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J. Neurophysiol. 36, 61-78 (1973).
2. McCormick, D.A. et al. Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb. Cortex 13, 1219-1231 (2003).
3. Shu, Y., Hasenstaub, A. & McCormick, D.A. Turning on and off recurrent balanced cortical activity. Nature 423, 288-293 (2003).
4. Camperi, M. & Wang, X.J. A model of visuospatial working memory in prefrontal cortex: recurrent network and cellular bistability. J. Comput. Neurosci. 5, 383-405 (1998).
5. Marder, E., Abbott, L.F., Turrigiano, G.G., Liu, Z. & Golowasch, J. Memory from the dynamics of intrinsic membrane currents. Proc. Natl. Acad. Sci. USA 93, 13481-13486 (1996).
6. Llinas, R. & Sugimori, M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.) 305, 171-195 (1980).
7. Heyward, P., Ennis, M., Keller, A. & Shipley, M.T. Membrane bistability in olfactory bulb mitral cells. J. Neurosci. 21, 5311-5320 (2001).
8. Lee, R.H. & Heckman, C.J. Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J. Neurophysiol. 80, 583-593 (1998).
9. Egorov, A.V., Hamam, B.N., Fransen, E., Hasselmo, M.E. & Alonso, A.A. Graded persistent activity in entorhinal cortex neurons. Nature 420, 173-178 (2002).
10. Koulakov, A.A., Raghavachari, S., Kepecs, A. & Lisman, J.E. Model for a robust neural integrator. Nat. Neurosci. 5, 775-782 (2002).
11. Goldman, M.S., Levine, J.H., Major, G., Tank, D.W. & Seung, H.S. Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron. Cereb. Cortex 13, 1185-1195 (2003).
12. Loewenstein, Y. & Sompolinsky, H. Temporal integration by calcium dynamics in a model neuron. Nat. Neurosci. 6, 961-967 (2003).
13. Hausser, M. & Clark, B.A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678 (1997).
14. Ito, M. The Cerebellum and Neural Control (Raven, New York, 1984).
15. Williams, S.R., Christensen, S.R. Stuart, G J. & Häusser, M. Membrane potential bistability is controlled by the hyperpolarization-activated current I(H) in rat cerebellar Purkinje neurons in vitro. J. Physiol. (Lond.) 539, 469-483 (2002).
16. Hartigan, J.A. & Hartigan, P.M. The dip test of unimodality. Ann. Stat. 13, 70-84 (1985).
17. Chadderton, P., Margrie, T.W. & Hausser, M. Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860 (2004).
18. Armstrong, D.M. & Rawson, J.A. Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J. Physiol. (Lond.)289, 425-448 (1979).
19. Jorntell, H. & Ekerot, C.F. Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J. Neurosci. 23, 9620-9631 (2003).
20. Brown, I.E. & Bower, J.M. Congruence of mossy fiber and climbing fiber tactile projections in the lateral hemispheres of the rat cerebellum. J. Comp. Neurol. 429, 59-70 (2001).
21. Rapp, M., Segev, I. & Yarom, Y. Physiology, morphology and detailed passive models of guinea-pig cerebellar Purkinje cells. J. Physiol. (Lond.) 474, 101-118 (1994).
22. Chang, W., Strahlendorf, J.C. & Strahlendorf, H.K. Ionic contributions to the oscillatory firing activity of rat Purkinje cells in vitro. Brain Res. 614, 335-341 (1993).
23. Hounsgaard, J. & Midtgaard, J. Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro. J. Physiol. (Lond.) 402, 731-749 (1988).
24. Bell, C.C. & Grimm, R.J. Discharge properties of Purkinje cells recorded on single and double microelectrodes. J. Neurophysiol. 32, 1044-1055 (1969).
25. Brookhart, J.M., Moruzzi, G. & Snider, R.S. Spike discharges of single units in the cerebellar cortex. J. Neurophysiol. 13, 465-486 (1950).
26. McDevitt, C.J., Ebner, T.J. & Bloedel, J.R. The changes in Purkinje cell simple spike activity following spontaneous climbing fiber inputs. Brain Res. 237, 484-491 (1982).
27. Granit, R. & Phillips, C.G. Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J. Physiol. (Lond.) 133, 520-547 (1956).
28. Nacimiento, R.C. Spontaneous and evoked discharges of cerebellar Purkinje cells in the frog. in Neurobiology of Cerebellar Evolution and Development (ed. Llinas, R.) 373-395 (American Medical Assn., Chicago, 1969).
29. McCarley, R.W. & Hobson, J.A. Simple spike firing patterns of cat cerebellar Purkinje cells in sleep and waking. Electroencephalogr. Clin. Neurophysiol. 33, 471-483 (1972).
30. Edgley, S.A. & Lidierth, M. Step-related discharges of Purkinje cells in the paravermal cortex of the cerebellar anterior lobe in the cat. J. Physiol. (Lond.) 401, 399-415 (1988).
31. Hirata, Y. & Highstein, S.M. Analysis of the discharge pattern of floccular Purkinje cells in relation to vertical head and eye movement in the squirrel monkey. Prog. Brain Res. 124, 221-232 (2000).
32. Bauswein, E., Kolb, F.P. & Rubia, F.J. Cerebellar feedback signals of a passive hand movement in the awake monkey. Pflugers Arch. 402, 292-299 (1984).
33. Kobayashi, Y. et al. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys II. Complex spikes. J. Neurophysiol. 80, 832-848 (1998).
34. Williams, S.R., Toth, T.I., Turner, J.P., Hughes, S.W. & Crunelli, V. The 'window' component of the low threshold Ca2+ current produces input signal amplification and bistability in cat and rat thalamocortical neurones. J. Physiol. (Lond.) 505, 689-705 (1997).
35. Rawson, J.A. & Tilokskulchai, K. Repetitive firing of cerebellar Purkinje cells in response to impulse in climbing fibre afferents. Neurosci. Lett. 25, 131-135 (1981).
36. Sato, Y., Miura, A., Fushiki, H. & Kawasaki, T. Short-term modulation of cerebellar Purkinje cell activity after spontaneous climbing fiber input. J. Neurophysiol. 68, 2051-2062 (1992).
37. Rawson, J.A. & Tilokskulchai, K. Suppression of simple spike discharges of cerebellar Purkinje cells by impulses in climbing fibre afferents. Neurosci. Lett. 25, 125-130 (1981).
38. Ekerot, C.F. & Kano, M. Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res. 342, 357-360 (1985).
39. Mahon, S., Deniau, J.M. & Charpier, S. Relationship between EEG potentials and intracellular activity of striatal and cortico-striatal neurons; an in vivo study under different anesthetics. Cereb. Cortex 11, 360-373 (2001).
40. Rinzel, J. & Ermentrout, B. Analysis of Neural Excitability and Oscillations in Methods of Neuronal Modeling (eds. Koch, C. & Segev, I.) 251-291 (MIT Press, Cambridge, 1998).
41. Yuen, G.L., Hockberger, P.E. & Houk, J.C. Bistability in cerebellar Purkinje cell dendrites modelled with high- threshold calcium and delayed-rectifier potassium channels. Biol. Cybern. 73, 375-388 (1995).
42. Genet, S. & Delord, B. A biophysical model of nonlinear dynamics underlying plateau potentials and calcium spikes in Purkinje cell dendrites. J. Neurophysiol. 88, 2430-2444 (2002).
43. Llinas, R. & Sugimori, M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. (Lond.) 305, 197-213 (1980).
44. Ebner, T.J. & Bloedel, J.R. Role of climbing fiber afferent input in determining responsiveness of Purkinje cells to mossy fiber inputs. J. Neurophysiol. 45, 962-971 (1981).
45. 2+ influx in turtle Purkinje cell dendrites in vitro: role of a transient outward current. J. Neurophysiol. 70, 2455-2469 (1993).
46. Wang, S.S., Denk, W. & Häusser, M. Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3, 1266-1273 (2000).
47. Margrie, T.W., Brecht, M. & Sakmann, B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 444, 491-498 (2002).
48. Mann-Metzer, P. & Yarom, Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J. Neurosci. 19, 3298-3306 (1999).