Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Dec 15;505(Pt 3):727–747. doi: 10.1111/j.1469-7793.1997.727ba.x

On the nature of anomalous rectification in thalamocortical neurones of the cat ventrobasal thalamus in vitro.

S R Williams 1, J P Turner 1, S W Hughes 1, V Crunelli 1
PMCID: PMC1160048  PMID: 9457648

Abstract

1. Intracellular sharp electrode current clamp and discontinuous single electrode voltage clamp recordings were made from thalamocortical neurones (n = 57) of the cat ventrobasal thalamus in order to investigate the mechanism underlying anomalous rectification. 2. Under current clamp conditions, voltage-current (V-I) relationships in a potential range of -55 to -110 mV demonstrated anomalous rectification with two components: fast rectification, which controlled the peak of negative voltage deviations, and time-dependent rectification. Time-dependent rectification was apparent as a depolarizing sag generated during the course of negative voltage deviations, was first formed at potentials in the range -60 to -70 mV, and was sensitive to 3 mM Cs+ (n = 6). Similarly, under voltage clamp conditions, instantaneous and steady-state I-V relationships demonstrated anomalous rectification. A slowly activating inward current with an activation threshold in the range of -65 to -70 mV formed time-dependent rectification. This current was sensitive to Cs+ (3 mM) (n = 3) and had properties similar to the slow inward mixed cationic current (Ih). 3. 4-(N-Ethyl-N-phenylamino)-1,2-dimethyl-6-(methylamino)-pyrimidinium++ + chloride (ZD 7288) (100-300 microM) irreversibly blocked time-dependent rectification mediated by Ih (n = 23 of 25 neurones), and led to a hyperpolarization of the resting membrane potential (6.8 +/- 0.5 mV). In the presence of ZD 7288, V-I and I-V relationships, exhibited fast anomalous rectification, first activated from potential more negative than -80 mV. 4. Ba2+ (100 microM) (n = 8), in the continuous presence of ZD 7288, reversibly linearized peak V-I and instantaneous I-V relationships over a potential range of -70 to -120 mV, and led to a membrane depolarization (13.3 +/- 4.2 mV) or tonic inward current (192 +/- 36 pA). 5. The co-application of ZD 7288 and Ba2+ revealed a depolarizing sag in negative voltage deviations under current clamp conditions, or a large inward current with kinetics two to three times slower than those of Ih under voltage clamp conditions. This novel form of time-dependent rectification was first apparent at potentials more negative than about -85 mV, was sensitive to 5 mM Cs+ (n = 4), and is termed Ih,slow. Ih,slow tail currents reversed between -65.3 and -56.6 mV (with potassium acetate electrodes, n = 3) or -57.6 and -50.3 mV (with KCl electrodes, n = 3). 6. Computer simulations confirmed that the pattern of anomalous rectification in thalamocortical neurones of the cat ventrobasal thalamus is mediated by the concerted action of Ih and a Ba(2+)-sensitive current with properties similar to an inwardly rectifying K+ current (IKIR).

Full text

PDF
727

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bal T., von Krosigk M., McCormick D. A. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. J Physiol. 1995 Mar 15;483(Pt 3):665–685. doi: 10.1113/jphysiol.1995.sp020613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Banks M. I., Pearce R. A., Smith P. H. Hyperpolarization-activated cation current (Ih) in neurons of the medial nucleus of the trapezoid body: voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. J Neurophysiol. 1993 Oct;70(4):1420–1432. doi: 10.1152/jn.1993.70.4.1420. [DOI] [PubMed] [Google Scholar]
  3. BoSmith R. E., Briggs I., Sturgess N. C. Inhibitory actions of ZENECA ZD7288 on whole-cell hyperpolarization activated inward current (If) in guinea-pig dissociated sinoatrial node cells. Br J Pharmacol. 1993 Sep;110(1):343–349. doi: 10.1111/j.1476-5381.1993.tb13815.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Constanti A., Galvan M. Fast inward-rectifying current accounts for anomalous rectification in olfactory cortex neurones. J Physiol. 1983 Feb;335:153–178. doi: 10.1113/jphysiol.1983.sp014526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crunelli V., Haby M., Jassik-Gerschenfeld D., Leresche N., Pirchio M. Cl- - and K+-dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. J Physiol. 1988 May;399:153–176. doi: 10.1113/jphysiol.1988.sp017073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crunelli V., Lightowler S., Pollard C. E. A T-type Ca2+ current underlies low-threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. J Physiol. 1989 Jun;413:543–561. doi: 10.1113/jphysiol.1989.sp017668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dong C. J., Werblin F. S. Inwardly rectifying potassium conductance can accelerate the hyperpolarizing response in retinal horizontal cells. J Neurophysiol. 1995 Dec;74(6):2258–2265. doi: 10.1152/jn.1995.74.6.2258. [DOI] [PubMed] [Google Scholar]
  8. Finkel A. S., Redman S. Theory and operation of a single microelectrode voltage clamp. J Neurosci Methods. 1984 Jun;11(2):101–127. doi: 10.1016/0165-0270(84)90029-3. [DOI] [PubMed] [Google Scholar]
  9. Gay L. A., Stanfield P. R. Cs(+) causes a voltage-dependent block of inward K currents in resting skeletal muscle fibres. Nature. 1977 May 12;267(5607):169–170. doi: 10.1038/267169a0. [DOI] [PubMed] [Google Scholar]
  10. Hagiwara S., Miyazaki S., Moody W., Patlak J. Blocking effects of barium and hydrogen ions on the potassium current during anomalous rectification in the starfish egg. J Physiol. 1978 Jun;279:167–185. doi: 10.1113/jphysiol.1978.sp012338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hagiwara S., Miyazaki S., Rosenthal N. P. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J Gen Physiol. 1976 Jun;67(6):621–638. doi: 10.1085/jgp.67.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harris N. C., Constanti A. Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J Neurophysiol. 1995 Dec;74(6):2366–2378. doi: 10.1152/jn.1995.74.6.2366. [DOI] [PubMed] [Google Scholar]
  13. Hu B. Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. J Physiol. 1995 Feb 15;483(Pt 1):167–182. doi: 10.1113/jphysiol.1995.sp020576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Karschin C., Dissmann E., Stühmer W., Karschin A. IRK(1-3) and GIRK(1-4) inwardly rectifying K+ channel mRNAs are differentially expressed in the adult rat brain. J Neurosci. 1996 Jun 1;16(11):3559–3570. doi: 10.1523/JNEUROSCI.16-11-03559.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Larkman P. M., Kelly J. S. Ionic mechanisms mediating 5-hydroxytryptamine- and noradrenaline-evoked depolarization of adult rat facial motoneurones. J Physiol. 1992 Oct;456:473–490. doi: 10.1113/jphysiol.1992.sp019347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lu Z., MacKinnon R. Electrostatic tuning of Mg2+ affinity in an inward-rectifier K+ channel. Nature. 1994 Sep 15;371(6494):243–246. doi: 10.1038/371243a0. [DOI] [PubMed] [Google Scholar]
  17. Mayer M. L., Westbrook G. L. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J Physiol. 1983 Jul;340:19–45. doi: 10.1113/jphysiol.1983.sp014747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McCormick D. A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol. 1992 Oct;39(4):337–388. doi: 10.1016/0301-0082(92)90012-4. [DOI] [PubMed] [Google Scholar]
  19. McCormick D. A., Pape H. C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol. 1990 Dec;431:291–318. doi: 10.1113/jphysiol.1990.sp018331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nisenbaum E. S., Wilson C. J. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci. 1995 Jun;15(6):4449–4463. doi: 10.1523/JNEUROSCI.15-06-04449.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pape H. C. Specific bradycardic agents block the hyperpolarization-activated cation current in central neurons. Neuroscience. 1994 Mar;59(2):363–373. doi: 10.1016/0306-4522(94)90602-5. [DOI] [PubMed] [Google Scholar]
  22. Sherman S. M., Koch C. The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res. 1986;63(1):1–20. doi: 10.1007/BF00235642. [DOI] [PubMed] [Google Scholar]
  23. Solomon J. S., Doyle J. F., Burkhalter A., Nerbonne J. M. Differential expression of hyperpolarization-activated currents reveals distinct classes of visual cortical projection neurons. J Neurosci. 1993 Dec;13(12):5082–5091. doi: 10.1523/JNEUROSCI.13-12-05082.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Solomon J. S., Nerbonne J. M. Two kinetically distinct components of hyperpolarization-activated current in rat superior colliculus-projecting neurons. J Physiol. 1993 Sep;469:291–313. doi: 10.1113/jphysiol.1993.sp019815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Spain W. J., Schwindt P. C., Crill W. E. Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1987 May;57(5):1555–1576. doi: 10.1152/jn.1987.57.5.1555. [DOI] [PubMed] [Google Scholar]
  26. Staley K. The role of an inwardly rectifying chloride conductance in postsynaptic inhibition. J Neurophysiol. 1994 Jul;72(1):273–284. doi: 10.1152/jn.1994.72.1.273. [DOI] [PubMed] [Google Scholar]
  27. Standen N. B., Stanfield P. R. A potential- and time-dependent blockade of inward rectification in frog skeletal muscle fibres by barium and strontium ions. J Physiol. 1978 Jul;280:169–191. doi: 10.1113/jphysiol.1978.sp012379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Standen N. B., Stanfield P. R. Potassium depletion and sodium block of potassium currents under hyperpolarization in frog sartorius muscle. J Physiol. 1979 Sep;294:497–520. doi: 10.1113/jphysiol.1979.sp012943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Steriade M., Deschênes M., Domich L., Mulle C. Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol. 1985 Dec;54(6):1473–1497. doi: 10.1152/jn.1985.54.6.1473. [DOI] [PubMed] [Google Scholar]
  30. Steriade M., Dossi R. C., Nuñez A. Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. J Neurosci. 1991 Oct;11(10):3200–3217. doi: 10.1523/JNEUROSCI.11-10-03200.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Steriade M., McCormick D. A., Sejnowski T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science. 1993 Oct 29;262(5134):679–685. doi: 10.1126/science.8235588. [DOI] [PubMed] [Google Scholar]
  32. Sutor B., Hablitz J. J. Influence of barium on rectification in rat neocortical neurons. Neurosci Lett. 1993 Jul 9;157(1):62–66. doi: 10.1016/0304-3940(93)90643-y. [DOI] [PubMed] [Google Scholar]
  33. Turner J. P., Anderson C. M., Williams S. R., Crunelli V. Morphology and membrane properties of neurones in the cat ventrobasal thalamus in vitro. J Physiol. 1997 Dec 15;505(Pt 3):707–726. doi: 10.1111/j.1469-7793.1997.707ba.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tóth T., Crunelli V. Computer simulation of the pacemaker oscillations of thalamocortical cells. Neuroreport. 1992 Jan;3(1):65–68. doi: 10.1097/00001756-199201000-00017. [DOI] [PubMed] [Google Scholar]
  35. Uchimura N., Cherubini E., North R. A. Inward rectification in rat nucleus accumbens neurons. J Neurophysiol. 1989 Dec;62(6):1280–1286. doi: 10.1152/jn.1989.62.6.1280. [DOI] [PubMed] [Google Scholar]
  36. Van Bogaert P. P., Goethals M., Simoens C. Use- and frequency-dependent blockade by UL-FS 49 of the if pacemaker current in sheep cardiac Purkinje fibres. Eur J Pharmacol. 1990 Oct 9;187(2):241–256. doi: 10.1016/0014-2999(90)90011-t. [DOI] [PubMed] [Google Scholar]
  37. Williams S. R., Turner J. P., Crunelli V. Gamma-hydroxybutyrate promotes oscillatory activity of rat and cat thalamocortical neurons by a tonic GABAB, receptor-mediated hyperpolarization. Neuroscience. 1995 May;66(1):133–141. doi: 10.1016/0306-4522(94)00604-4. [DOI] [PubMed] [Google Scholar]
  38. Williams S. R., Tóth 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. 1997 Dec 15;505(Pt 3):689–705. doi: 10.1111/j.1469-7793.1997.689ba.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Womble M. D., Moises H. C. Hyperpolarization-activated currents in neurons of the rat basolateral amygdala. J Neurophysiol. 1993 Nov;70(5):2056–2065. doi: 10.1152/jn.1993.70.5.2056. [DOI] [PubMed] [Google Scholar]
  40. Yamaguchi K., Nakajima Y., Nakajima S., Stanfield P. R. Modulation of inwardly rectifying channels by substance P in cholinergic neurones from rat brain in culture. J Physiol. 1990 Jul;426:499–520. doi: 10.1113/jphysiol.1990.sp018151. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES