Electrophysiological and Morphological Classification of Inhibitory Interneurons in Layer II/III of the Rat Visual Cortex

  • Rhie, Duck-Joo (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Kang, Ho-Young (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Ryu, Gyeong-Ryul (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Kim, Myung-Jun (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Yoon, Shin-Hee (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Hahn, Sang-June (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Min, Do-Sik (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Jo, Yang-Hyeok (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Kim, Myung-Suk (Department of Physiology, College of Medicine, The Catholic University of Korea)
  • Published : 2003.12.21

Abstract

Interneuron diversity is one of the key factors to hinder understanding the mechanism of cortical neural network functions even with their important roles. We characterized inhibitory interneurons in layer II/III of the rat primary visual cortex, using patch-clamp recording and confocal reconstruction, and classified inhibitory interneurons into fast spiking (FS), late spiking (LS), burst spiking (BS), and regular spiking non-pyramidal (RSNP) neurons according to their electrophysiological characteristics. Global parameters to identify inhibitory interneurons were resting membrane potential (>-70 mV) and action potential (AP) width (<0.9 msec at half amplitude). FS could be differentiated from LS, based on smaller amplitude of the AP (<∼50 mV) and shorter peak-to-trough time (P-T time) of the afterhyperpolarization (<4 msec). In addition to the shorter AP width, RSNP had the higher input resistance (>200 $M{Omega}$) and the shorter P-T time (<20 msec) than those of regular spiking pyramidal neurons. Confocal reconstruction of recorded cells revealed characteristic morphology of each subtype of inhibitory interneurons. Thus, our results provide at least four subtypes of inhibitory interneurons in layer II/III of the rat primary visual cortex and a classification scheme of inhibitory interneurons.

Keywords

References

  1. Ali AB, Deuchars J, Pawelzik H, Thomson AM. CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J Physiol 507: 201-217, 1998 https://doi.org/10.1111/j.1469-7793.1998.201bu.x
  2. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38: 805-817, 2003 https://doi.org/10.1016/S0896-6273(03)00300-3
  3. Buhl EH, Tamas G, Fisahn A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 513: 117-126, 1998. https://doi.org/10.1111/j.1469-7793.1998.117by.x
  4. Chu Z, Galarreta M, Hestrin S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23: 96-102, 2003 https://doi.org/10.1523/JNEUROSCI.23-01-00096.2003
  5. Douglas R, Martin K. Neocortex. In: Shepherd GM. Ed, The synaptic organization of the brain. 4th ed, Oxford, New York, p 459-509, 1998
  6. Erisir A, Lau D, Rudy B, Leonard CS. Function of specific K($^+$) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82: 2476-2489, 1999
  7. Freund TF, Buzsaki G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996. https://doi.org/10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-I
  8. Gupta A, Wang Y, Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273-278, 2000 https://doi.org/10.1126/science.287.5451.273
  9. Katz B, Miledi R. The role of calcium in neuromuscular facilitation. J Physiol 195: 481-492, 1968 https://doi.org/10.1113/jphysiol.1968.sp008469
  10. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15: 2638-2655, 1995 https://doi.org/10.1523/JNEUROSCI.15-04-02638.1995
  11. Kawaguchi Y, Kubota Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28kimmunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387-396, 1993 https://doi.org/10.1152/jn.1993.70.1.387
  12. Kawaguchi Y, Kubota Y. Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptidecontaining cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16: 2701-2715, 1996 https://doi.org/10.1523/JNEUROSCI.16-08-02701.1996
  13. Losonczy A, Zhang L, Shigemoto R, Somogyi P, Nusser Z. Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones. J Physiol 542: 193-210, 2002 https://doi.org/10.1113/jphysiol.2002.020024
  14. Mainen ZF, Sejnowski TJ. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382: 363-366, 1996 https://doi.org/10.1038/382363a0
  15. McBain CJ, Fisahn A. Interneurons unbound. Nat Rev Neurosci 2: 11-23, 2001 https://doi.org/10.1038/35049047
  16. McGann JP, Moyer JR Jr, Brown TH. Predominance of late-spiking neurons in layer VI of rat perirhinal cortex. J Neurosci 21: 4969 -4976, 2001 https://doi.org/10.1523/JNEUROSCI.21-14-04969.2001
  17. Miller MW. The migration and neurochemical differentiation of gamma-aminobutyric acid (GABA)-immunoreactive neurons in rat visual cortex as demonstrated by a combined immunocytochemical- autoradiographic technique. Brain Res 393: 41- 46, 1986
  18. Mott DD, Dingledine R. Interneuron Diversity series: Interneuron research--challenges and strategies. Trends Neurosci 26: 484-488, 2003 https://doi.org/10.1016/S0166-2236(03)00200-5
  19. Mountcastle VB, Talbot WH, Sakata H, Hyvarinen J. Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32: 452-484, 1969 https://doi.org/10.1152/jn.1969.32.3.452
  20. Nowak LG, Azouz R, Sanchez-Vives MV, Gray CM, McCormick DA. Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J Neurophysiol 89: 1541-1566, 2003 https://doi.org/10.1152/jn.00580.2002
  21. Parnavelas JG. Development of GABA-containing neurons in the visual cortex. Prog Brain Res 90: 523-537, 1992 https://doi.org/10.1016/S0079-6123(08)63629-8
  22. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285, 1998 https://doi.org/10.1038/1092
  23. Rozas C, Frank H, Heynen AJ, Morales B, Bear MF, Kirkwood A. Developmental inhibitory gate controls the relay of activity to the superficial layers of the visual cortex. J Neurosci 21: 6791- 6801, 2001
  24. Rudy B, McBain CJ. Kv3 channels: voltage-gated K$^+$ channels designed for high-frequency repetitive firing. Trends Neurosci 24: 517-526, 2001 https://doi.org/10.1016/S0166-2236(00)01892-0
  25. Sanchez-Vives MV, Nowak LG, McCormick DA. Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J Neurosci 20: 4286-4299, 2000
  26. Scanziani M, Gahwiler BH, Charpak S. Target cell-specific modulation of transmitter release at terminals from a single axon. Proc Natl Acad Sci USA 95: 12004-12009, 1998 https://doi.org/10.1073/pnas.95.20.12004
  27. Sillito AM. Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol 289: 33-53, 1979 https://doi.org/10.1113/jphysiol.1979.sp012723
  28. Singer W. Development and plasticity of cortical processing architectures. Science 270: 758-764, 1995 https://doi.org/10.1126/science.270.5237.758
  29. Somogyi P, Tamas G, Lujan R, Buhl EH. Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26: 113-135, 1998 https://doi.org/10.1016/S0165-0173(97)00061-1
  30. Tamas G, Szabadics J, Somogyi P. Cell type- and subcellular position- dependent summation of unitary postsynaptic potentials in neocortical neurons. J Neurosci 22: 740-747, 2002 https://doi.org/10.1523/JNEUROSCI.22-03-00740.2002