Summary
In 17 frogs (Rana esculenta var ridibunda) immobilised with succinyl choline the optic tectal surface was stimulated by trains of electrical pulses or by a flash to the contralateral eye. Sustained potential shifts (SPSs) and changes in extracellular potassium concentration (Δ [K+]0) were simultaneously recorded.
In response to electrical stimulation SPSs of maximal amplitudes (1.19±0.1 mV) were recorded between 50 and 200 μm in depth and maximal Δ[K+]0 (0.69 ±0.08 mM) between 100 and 350 μm. The changes of SPS and Δ[K+]0 showed a close similarity in experiments with changes in voltage, pulse duration and frequency of stimuli within a train. The induced SPS had a duration of 28±1.54 s, the Δ [K+]0 of 32±1.23 s.
The flash stimulus induced an SPS and Δ [K+]0 of maximal amplitudes between 50 and 200 μm in depth with values of 0.57±0.1 mV and 0.29±0.03 mM respectively. An additional wave with a latency of ca 1 s and a duration of ca 3 s arose on the background of the SPS to a flash stimulus, associated with an additional increase in [K+]0.
It is considered that the accumulation of K+ in extra-cellular space, with neuronal activity, results in depolarization of radial processes of ependymal glia. This is reflected in the neuropil of the upper layers of the optic tectum as an SPS.
Similar content being viewed by others
References
Buser P (1955) Etude de l'activité électrique du lobe optique des vertébrés inférieurs. J Physiol (Paris) 47:737–768
Cajal SR (1955) Histologie du système nerveux de l'homme et des vertébrés. Tome II. Institute Ramón y Cajal Madrid, 993 pp
Ewert J-P (1976) The visual system of the toad: behavioural and physiological studies on a pattern recognition system. In: Fite KV (ed) The amphibian visual system. Academic Press, New York San Francisco London, pp 141–202
Ewert J-P (1989) The release of visual behaviour in toads: stages of parallel/hierarchial information processing. In: Ewert J-P, Arbib MA (eds) Visuomotor coordination: amphibians, comparisons, models and robots. Plenum Press, New York London, 39–120
Fite KV, Scalia F (1976) Central visual pathways in the frog. In: Fite KV (ed) The amphibian visual system. Academic Press, New York San Francisco London, pp 87–118
Gardner-Medwin AR (1987) Assessment of the glial spatial buffer mechanism in rat brain, frog brain and retina. In: Roitbak AI (ed) Functions of neuroglia. Metsniereba Press, Tbilisi USSR, pp 138–145
Gianonatti C, Bodega G, Bardasano JL (1987) Neuroglia in the optic tectum in the toad Bufo bufo (Amphibia, Anura), first trials. J Hirnforsch 28:139–143
Heinemann U, Lux HX, Marciani MG, Holmeier G (1979) Slow potentials in relation to changes in extracellular potassium activity in the cortex of the cats. In: Speckman E-J, Caspers H (eds) Origin of cerebral field potentials. G. Thieme, Stuttgart, 33–48
Kuffler SW, Nicholls JG (1966) The physiology of neuroglial cells. Ergeb Physiol 57:1–90
Laming PR (1989) Central representation of arousal. In: Ewert J-P, Arbib MA (eds) Visuomotor coordination: Amphibians, comparisons, models and robots. Plenum Press, New York London, pp 693–727
Laming PR, Ewert J-P (1984) Visual unit, EEG and sustained potential shift responses to biologically significant stimuli in the brain of toads (Bufo bufo). J Comp Physiol A 154:89–101
Laming PR, Borchers H-W, Ewert J-P (1984) Visual unit, EEG and sustained potential shift responses in the brains of toads (Bufo bufo) during alert and defensive behaviour. Physiol Behav 32:463–468
Laming PR, Ocherashvili IV, Nicol AU (1991) Dendritic and sustained shifts in potential to electrical stimulation of the anuran tectal surface. Comp Biochem Physiol A 101A 1:91–96
Lázár G (1989) Cellular architecture and connectivity of the frog's optic tectum and pretectum. In: Ewert J-P, Arbib MA (eds) Visuomotor coordination: amphibians, comparisons, models and robots. Plenum Press, New York London, pp 175–199
Manteifel YB (1971) Slow negative wave of the evoked potential in the midbrain tectum of the frog. (In Russian). Neirofisiologiya (Kiev) 3:145–153
Manteifel YB (1974) Evoked potentials of the visual centre of amphibian midbrain. (In Russian). Nauka (Moscow), 176 pp
Manteifel YB, Dyachkova LN (1974) Axo-axonic synapses in the optic tectum of Rana temporaria. (In Russian). Neirofisiologiya 6:37–43
Matsumoto N (1989) Morphological and physiological studies of tectal and pretectal neurons in the frog. In: Ewert J-P, Arbib MA (eds) Visual coordination: amphibians, comparisons, models and robots. Plenum Press, New York London, pp 201–222
Ransom BR, Connors BW (1987) Electrophysiology of ependymal cells in turtle cortex. In: Roitbak AI (ed) Functions of neuroglia. Metsniereba, Tbilisi, pp 81–88
Roitbak AI (1983) Neuroglia: Eigenschaften, Funktionen, Bedeutung. VEB G. Fischer, Jena, 210 pp
Roitbak AI, Fanardjian VV (1981) Depolarization of cortical glial cells in response to electrical stimulation of the cortical surface. Neuroscience 6:2529–2537
Roitbak AI, Machek J, Pavlik V, Bobrov AV, Ocherashvili IV (1981) The slow component of the direct cortical response and extracellular potassium. In: Sykova E, Hnik P, Vyklicky L (eds) Ion-selective microelectrodes and their use in excitable tissues. Plenum Press, New York, pp 267–272
Roitbak AI, Machek I, Pavlik V, Ocherashvili IV, Kapel RG (1984) Changes in the concentration of extracellular potassium and slow negative potentials in the cerebral cortex. (In Russian). In: Kostyuk PG (ed) Investigation of the mechanisms of nervous activity. Nauka, Moscow, pp 22–32
Roitbak AI, Fanardjian VV, Melkonyan DS, Melkonyan AA (1987) Contribution of glia and neurons to the surface-negative potentials of the cerebral cortex during its electrical stimulation. Neuroscience 20:1057–1067
Sick TJ, Kreisman NR (1981) Potassium ion homeostasis in amphibian brain: Contribution of active transport and oxidative metabolism. J Neurophysiol 45:998–1012
Simpson JI (1976) Functional synaptology of the spinal cord. In: Llinás R, Precht W (eds) Frog neurobiology — a handbook. Springer, Berlin Heidelberg New York, pp 728–749
Székely C, Lázár G (1976) Cellular and synaptic architecture of the optic tectum. In: Llinás R, Precht W (eds) Frog neurobiology — a handbook. Springer, Berlin Heidelberg New York, pp 407–434
Zagorulko TM (1958) Electrophysiological investigation of the activity of the visual analyser in the frog. (In Russian). Fiziologichesky Zurnal 44:928–937
Author information
Authors and Affiliations
Additional information
We would like to dedicate this article to the memory of Alexander Roitbak who died as a result of a tragic accident while this paper was in press. He will be remembered fondly especially for his contributions to understanding of the functions of Neuroglia. E.V.O., P.R.L., T.A.R.
Rights and permissions
About this article
Cite this article
Roitbak, A.I., Ocherashvili, E.V., Laming, P.R. et al. Stimulus-evoked slow potential shifts and changes in [K+]0 of the frog optic tectum. J Comp Physiol A 170, 327–333 (1992). https://doi.org/10.1007/BF00191421
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00191421