Advertisement

Experimental Brain Research

, Volume 81, Issue 2, pp 241–256 | Cite as

Optical recording of epileptiform voltage changes in the neocortical slice

  • B. Albowitz
  • U. Kuhnt
  • L. Ehrenreich
Regular Papers

Summary

Voltage sensitive probes were used to monitor the development, distribution, and spread of epileptiform potentials with a photodiode array in neocortical slices of guinea pigs. Epileptiform activity was induced by bath application of bicuculline-methiodide or 3,4-diaminopyridine and electrical stimulation of white matter or cortical layer I. Stimulation evoked a primary or early potential which was followed by a delayed epileptiform potential with a larger spatial extent. Shape, duration and amplitude of the delayed epileptiform potential varied strongly among slices and across the recording area and could reach largest amplitudes at a distance from the stimulation point. At a specific recording site, however, with repeated stimulation, potentials were generated in a stereotyped way. Intracellularly recorded delayed epileptiform potentials corresponded very closely at least to the early part of the optical response. Epileptiform activity appeared in layer III as soon as the primary potential reached sufficient amplitude there. Apart from this relationship, the distribution and spread of maximal amplitudes of delayed epileptiform potentials were segregated from those of early potentials. Early potentials reached maximal amplitudes close to the stimulation site. In contrast, the largest amplitudes of delayed epileptiform potentials were always found in layer III. A second maximum occasionally occurred in layer V. The horizontal amplitude distribution of epileptiform potentials was asymmetric, i.e. amplitudes increased to one side and decreased to the other. Early potential maxima spread from deeper to upper layers when initiated by white matter stimulation and from upper to deeper layers when initiated by layer I stimulation. In contrast, delayed epileptiform potentials always spread from layer III to lower layers and to the sides. Velocity of spread of early potentials and delayed epileptiform potentials differed systematically along the vertical and horizontal axis. The distribution of maximal amplitudes, shape, and pattern of spread of epileptiform potentials was the same whether white matter or layer I was stimulated. The independence of delayed epileptiform potential characteristics from the point of stimulation and from early potential characteristics suggests that epileptiform activity is determined by intrinsic properties of the cortex and not by afferent activation.

Key words

Optical recording Voltage sensitive probe Neocortical slice Epilepsy Guinea pig 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albowitz B, Gasteiger EL (1988) Laminar sensitivity of different neocortical areas to electrically induced epileptiform after-discharge. In: Elsner N, Barth GB (eds) Sense organs. Thieme, Stuttgart New York, p 116Google Scholar
  2. Albowitz B, Kuhnt U (1989) Optical recordings reveal the spatiotemporal distribution of epileptic activity in the neocortical slice. Eur J Neurosci Suppl 2:58Google Scholar
  3. Baldino F Jr, Wolfson B, Heinemann U, Gutnick MJ (1986) An NMDA receptor antagonist reduces bicuculline-induced depolarization shifts in neocortical expiant cultures. Neurosci Lett 70:101–105Google Scholar
  4. Campbell AW, Holmes O (1984) Bicuculline epileptogenesis in the rat. Brain Res 241:239–246Google Scholar
  5. Chagnac-Amitai Y, Connors BW (1989) Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61:747–758Google Scholar
  6. Chatt AB, Ebersole JS (1982) The laminar sensitivity of cat striate cortex to penicillin induced epileptogenesis. Brain Res 241:382–387Google Scholar
  7. Chervin RD, Pierce PA, Connors BW (1988) Periodicity and directionality in the propagation of epileptiform discharge across neocortex. J Neurophysiol 60:1695–1713Google Scholar
  8. Cohen LB, Landowne D, Shrivastav B, Ritchie M (1970) Changes in fluorescence of squid axons during activity. Biol Bull 139:418–419Google Scholar
  9. Cohen LB, Salzberg BM, Davila HV, Ross WN, Landowne D, Waggoner AS, Wang CH (1974) Changes in axon fluorescence during activity: molecular probes of membrane potential. J Membr Biol 19:1–36Google Scholar
  10. Connors BW (1984) Initiation of synchronized neuronal bursting in neocortex. Nature 310:685–687Google Scholar
  11. Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48:1302–1320Google Scholar
  12. Ebersole JS, Chatt AB (1981) Toward a unified theory of focal penicillin epileptogenesis: an intracortical evoked potential investigation. Epilepsia 22:347–363Google Scholar
  13. Ebersole JS, Chatt AB (1984) Laminar interactions during neocortical epileptogenesis. Brain Res 298:253–271Google Scholar
  14. Fisken RA, Garey LY, Powell TPS (1975) The intrinsic, association and commissural connections of area 17 of the visual cortex. Philos Trans R Soc (Lond) 272:487–536Google Scholar
  15. Fleischhauer K, Petsche H, Wittkowski W (1972) Vertical bundles of dendrites in the neocortex. Z Anat Entwickl Gesch 136:213–23Google Scholar
  16. Fox K, Sato H, Daw N (1989) The location and function of NMDA receptors in cat and kitten visual cortex. J Neurosci 9:2443–2454Google Scholar
  17. Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116–1133Google Scholar
  18. Goldensohn ES, Salazar AM (1986) Temporal and spatial distribution of intracellular potentials during generation and spread of epileptogenic discharge. Adv Neurol 44:559–582Google Scholar
  19. Grinvald A, Cohen LB, Lesher S, Boyle MB (1981) Simulataneous optical monitoring of activity of many neurons in invertebrate ganglia, using a 124 element ‘photodiode’ array. J Neurophysiol 45:829–840Google Scholar
  20. Grinvald A, Manker A, Segal M (1982) Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J Physiol (London) 333:269–291Google Scholar
  21. Grinvald A, Anglister L, Freeman JA, Hildesheim R, Manker A (1984) Real-time optical imaging of naturally evoked electrical activity in the intact frog brain. Nature 308:848–850Google Scholar
  22. Grinvald A, Segal M, Kuhnt U, Hildesheim R, Manker A, Anglister L, Freeman JA (1986) Real-time optical mapping of neuronal activity in vertebrate CNS in vitro and in vivo. Soc Gen Physiol Ser 40:165–197Google Scholar
  23. Grinvald A, Frostig RD, Lieke E, Hidesheim R (1988) Optical imaging of neuronal activity. Physiol Rev 68:1285–1366Google Scholar
  24. Gutnick MJ, Connors BW, Prince DA (1982) Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 48:1321–1335Google Scholar
  25. Gutnick MJ, Wolfson B, Baldino F (1989) Synchronized neuronal activities in neocortical expiant cultures. Exp Brain Res 76:131–140Google Scholar
  26. Holmes G, Lockton W (1982) Penicillin epileptogenesis in the rat: diffusion and the differential laminar sensitivity of the cortex cerebri. Brain Res 231:131–141Google Scholar
  27. Kisvárdy ZF, Martin KAC, Freund TF, Maglóczky ZS, Whitteridge D, Somogyi P (1986) Synaptic targets of HRP-filled layer III pyramidal cells in cat striate cortex. Exp Brain Res 64:541–552Google Scholar
  28. Konnerth A, Orkand RK (1986) Voltage-sensitive dyes measure potential changes in axons and glia of the frog optic nerve. Neurosci Lett 66:49–54Google Scholar
  29. Konnerth A, Orkand PM, Orkand RK (1988) Optical recording of electrical activity from axons and glia of frog optic nerve: potentiometric dye responses and morphometrics. Glia 1:225–232Google Scholar
  30. Kuhnt U, Grinvald A (1982) 4-AP induces presynaptic changes in the hippocampal slices as measured by optical recording and voltage-sensitive dyes. Pflügers Arch Suppl 394:R45Google Scholar
  31. Kuhnt U, Ehrenreich L (1988) Mapping of evoked electrical activity in neocortical slices using optical recording techniques. Soc Neurosci Abstr 14:1122Google Scholar
  32. Kusske JA (1976) Interaction between thalamus and cortex in experimental epilepsy in the cat. Exp Neurol 50:568–578Google Scholar
  33. Lev-Ram V, Grinvald A (1986) Ca++ and K+ dependent communication between central nervous system myelinated axons and oligodendrocytes revealed by voltage-sensitive dyes. Proc Natl Acad Sci USA 83:6651–6655Google Scholar
  34. Lockton JW, Holmes O (1980) Site of the initiation of penicillininduced epilepsy in the cortex cerebri of the rat. Brain Res 190:301–304Google Scholar
  35. Lockton JW, Holmes O (1983) Penicillin epilepsy in the rat: the responses of different layers of the cortex cerebri. Brain Res 258:79–89Google Scholar
  36. London JA, Cohen LB, Wu J-Y (1989) Optical recordings of the cortical response to whisker stimulation before and after the addition of an epileptogenic agent. J Neurosci 9:2182–2190Google Scholar
  37. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37–100Google Scholar
  38. Orbach HS, Cohen LB, Grinvald A (1985) Optical mapping of electrical activity in rat somatosensory and visual cortex. J Neurosci 5:1886–1895Google Scholar
  39. Petsche H, Pockberger H, Rappelsberger P (1984) On the search for the sources of the electroencephalogram. Neuroscience 11:1–27Google Scholar
  40. Prince DA (1983) Ionic mechanisms in cortical and hippocampal epileptogenesis. In: Jasper HH, van Gelder NM (eds) Basic mechanisms of neuronal hyperexcitability. Liss, New York, pp 217–243Google Scholar
  41. Pockberger H, Rappelsberger P, Petsche H (1984a) Penicillin-induced epileptic phenomena in the rabbit's neocortex. I. The development of interictal spikes after epicortical application of penicillin. Brain Res 309:247–260Google Scholar
  42. Pockberger H, Rappelsberger P, Petsche H (1984b) Penicillininduced epileptic phenomena in the rabbit's neocortex. II. Laminar specific generation of interictal spikes after the application of penicillin to different cortical depth. Brain Res 309:261–269Google Scholar
  43. Ross WN, Salzberg BM, Cohen LB, Grinvald A, Davila HV, Waggoner AS, Wang CH (1977) Changes in absorption, fluorescence, dichroism, and birefringence in stained giant axons: optical measurement of membrane potential. J Membr Biol 33:141–183Google Scholar
  44. Thomson AM, West DC (1986) N-methylaspartate receptors mediate epileptiform activity evoked in some, but not all, conditions in rat neocortical slices. Neuroscience 19:1161–1177Google Scholar
  45. Taylor CP, Dudek FE (1984) Synchronization without active chemical synapses during hippocampal afterdischarges. J Neurophysiol 52:143–155Google Scholar
  46. Traub RD, Knowles WD, Miles R, Wong RKS (1984) Synchronized afterdischarge in the hippocampus: simulation studies of the cellular mechanism. Neuroscience 12:1191–1200Google Scholar
  47. Traub RD, Miles R, Wong RKS (1987a) Models of synchronized hippocampal bursts in the presence of inhibition. I. Single population events. J Neurophysiol 58:739–751Google Scholar
  48. Traub RD, Knowles WD, Miles R, Wong RKS (1987b) Models of the cellular mechanism underlying propagation of epileptiform activity in the CA2–CA3 region of the hippocampal slice. Neuroscience 21:457–470Google Scholar
  49. Wong RKS, Prince DA, Basbaum AI (1979) Intradendritic recordings from hippocampal neurons. Proc Nat Acad Sci USA 76:986–990Google Scholar
  50. Yaari Y, Konnerth A, Heinemann U (1983) Spontaneous epileptiform activity of CA1 hippocampal neurons in low extracellular calcium solution. Exp Brain Res 51:153–156Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • B. Albowitz
    • 1
  • U. Kuhnt
    • 1
  • L. Ehrenreich
    • 1
  1. 1.Department of NeurobiologyMax-Planck-Institute for Biophysical ChemistryGöttingenFederal Republic of Germany

Personalised recommendations