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Intrageniculate terminal depolarization of the cats retinal ganglion cell axons during reserpine-induced PGO-spike
.Ye,,royho~rrru‘oioyl. 1974. 13. Il91- 1193. Pergamon Prec,. Prmted ,n Cit. Bntam
INTRAGENICULATE TERMINAL DEPOLARIZATION THE CAT’S RETINAL GANGLION CELL AXONS DURING RESERPINE-INDUCED PGO-SPIKE
OF
T. SATOH,N. KANAMORI and L. M. VERNON Department of Physiology. School of Dentistry, Aichi-Gakuin University, Nagoya. 464, Japan
(Accepted I Jlrrle 1974)
Summary-Intrageniculate terminal depolarization of the retinal ganglion cell axons is enhanced during the occurrence of reserpine-induced ponto-geniculo-occipital-spikes (PGOK) in the cat immobilized with gallamine triethiodide, thus providing additional evidence for the functional similarity of PGO, to PGO-spikes occurring during REM sleep and arousal. It is suggested that during PGOa, one of the essential changes occurring in the lateral geniculate body is an alteration of the interaction between different retinal afferents.
Erratic field potential changes occurring synchronously with rapid eye movements have been recorded in a variety of brain areas involved in oculomotor and visual functions (JOUVET, 1969). According to the sites of their main occurrence, these potentials are generally called ponto-geniculo-occipital (PGO) spikes. As to the physiological significance of these spikes, feed-forward control of the oculomotor centre over the visual system has been hypothesized. In support of this idea, terminal depolarization of the retinal ganglion cell axons occurs synchronously with PGO-spikes during rapid eye movement (REM) sleep of the cat (IWAMA,KAWAMOTO, SAKAKURA and KASAMATSU,1966) and during saccadic eye movements of the awake monkey (FELDMAN and COHEN, 1968); thus suggesting presynaptic inhibition of the visual input during rapid eye movements. On the other hand, spike activity apparently similar to PGO-spikes of REM sleep and of arousal has been found in reserpine-treated cats (DELORME, JEANNEROD and JOUVET, 1965). Recent investigations have revealed that the reserpine-induced PGO-spike (PGOR) possesses several functional characteristics quite close to those of PGO-spikes found on other backgrounds (BROOKSand GERSHON, 1971; MUNSON and GRAHAM, 1971; SATOH, 1972).
The present investigation was undertaken to find out whether, during PGO,, there are changes at the retinal ganglion cell terminals, which are comparable to those observed during PGO-spikes of REM sleep and arousal. Cats were operated under ether anaesthesia. Reserpine, @5 mg/kg (Apoplon. Dai-ichi Seiyaku) was administered intravenously at least 3 hr before the start of the recording. After interruption of ether, the animal was immobilized with gallamine triethiodide (Teikoku Chemical) and submitted to artificial respiration. Pressure points and wounds were heavily infiltrated with long-lasting procaine chloride jelly. The rectal temperature was
i191
1192
T.
SATOH,
N.
KANAMOKIand L. M. V~KNON
maintained at 375°C. Rectangular pulses of 0.01 msec duration were delivered every 1 set through stimulating electrodes in the lateral geniculate body (LGB). Antidromically elicited compound action potentials were picked up monopolarly from the ipsilateral optic tract about 1 mm caudal to the optic chiasm. The reserpine-induced PGO spike was obtained bipolarly from the contralateral LGB.
LGB
OT
Fig. 1. Enhancement of amplitude of antidromic compound action potential during PGO, (right arrow) relative to control response (left arrow). UT; optic tract response to electrical stimulation of the ipsilateral LGB.
The responses obtained from the optic tract had l-3 peaks. The response with peak latency at about 0.8 msec could be most stably recorded. so the analysis was confined to that wave. Effect
of reserpne
- PGO upon
ant ldromic
response
32
L
RdR
5”
mz
Fig. 2. On the right, total number ofexperiments in which the enhancement ofantidromic response during PGOR was significant (hatched column) or non-significant (open column) at the level P < 0.05 (Student’s t-test). The number of measured responses associated or unassociated with PGOn was 35-85 (mostly 5C-60) in each experiment. The abscissa is the average degrees of increase in the optic tract response during PGO,.
When the test stimulus was given to the LGB during the occurrence of PGO,,, the amplitude of the optic tract response was increased in most occasions (Fig. 1). A summary of sites in the results obtained from 11 cats is found in Figure 2. Among the 46 stimulated the LGB, 32 gave an increase in response size during PGO,. The degree of increase varied considerably from experiment to experiment. This degree is dependent not only on the number of fibres receiving terminal depolarization, but also on the number of fibres which were stimulated at their axon stems, instead of the axon terminals. However, there was
Reserpine
PGO-spike
1193
a case in which the increase reached 40 per cent; indicating that the fibres undergoing an enhanced terminal depolarization during PGO, are fairly numerous. There were some experiments in which the response did not show any significant change during PGOK. In these experiments, a theoretical possibility is that the responses were produced mainly by stimulating the intrageniculate axon stems of the retinal ganglion cells. The present results show that the intrageniculate terminals of retinal ganglion cell axons are depolarized during PGO,. It follows that the functional role of PGO, in the LGB is quite similar to that of PGO-spikes during REM sleep and arousal. This is consistent with the data hitherto obtained that those three kinds of PGO-spikes possess many properties in common. SINCZII (1973) has observed terminal depolarization of retinal ganglion cell axons during PGO-like slow waves elicited by electrical stimulation of the mesencephalic reticular formation. He has concluded that the presence of presynaptic inhibition is questionable, since the transmission of the optic nerve impulses through the LGB was not impaired significantly during those waves. His conclusion raises a serious question about the physiological significance of the ganglion cell axon terminal depolarization which has been repeatedly observed in different experimental situations. However, detection of terminal depolarization by the excitability testing method of WALL (1958) does not prove conclusively that it is those fibres synapsing onto the principal cells of the LGB which are depolarized. If the depolarization were operating at axon branch terminals which are connected to LGB internuncial neurones not directly involved in the transmission of visual information to the visual cortex. it would be possible to obtain an enhanced antidromic response simultaneously with unimpaired transmission from the optic tract to the optic radiation. Furthermore, in view of the fact that the internuncial neurones are mostly inhibitory to the principal cells, the diminished excitation of the former during PGO,< would result in disinhibition of the latter, the occurrence of which has been deduced from the results of stimulation of the mesencephalic reticular formation (FUKLDA and IWAMA, 1971; SINGER, 1973). Therefore, it seems that during PGO, one of the essential changes occurring in the LGB would be an altered interaction between different retinal affercnts. rather than reduced transmission of visual information. REFERENCES BKOOKS, D. C. and &RSNOh, M. D. (1971). Eye movement potentials in the oculomotor and visual systems of the cat: a comparison of reserpine induced waves with those present during wakefulness and rapid eye movement sleep. Brain Rcs. 21: 223-239. DIXORME, F., JIIANNFROD.M. and JOYVET. M. (1965). Effets remarquables de la riserpine sur l’activite EEG phasique ponto-g&niculo-occipitale. C. I’. Siarlc. Sec. Biol. 15% 90@903. FELLNAN’, M. and COHEN. B. (1968). Electrical activity in the lateral geniculate body of the alert monkey associated with eye movements. J. Nrz~opl~~siol. 31: 455-466. FCKUUA. Y. and IWAMA, K. (1971). Reticular inhibition of internuncial cells in the rat lateral geniculate body. Brait] Rrs. 35: 107-l 18. IWAMA. K.. KAWAMOTO. T.. SAKAKURA, H. and KASAMATSU.T. (1966). Responsiveness of cat lateral geniculate at pre- and postsynaptic levels during natural sleep. Physiol. Behao. I: 45-53. JOIVIZ~, M. (1969). Biogenic amines and the states of sleep. Science. N.Y 163: 32-41. MUNSON. J. B. and GRAHAM. R. B. (1971). Lateral geniculate spikes in sleeping. awake, and reserpine-treated cats: correlated excitability changes in superior colliculus and related structures. EvpI Nru,ol. 31: 326-336. SATOH. T. (1972). Cortical responsiveness during reserpine-induced PGO-spike in the cat. lnt. J. Neurosci. 3: 201204. SINXR. W. (1973). Brain stem stimulation and the hypothesis of presynaptic inhibition in cat lateral geniculate nucleus. Bruin Res. 61: 55-68. WALL. P. D. (1958). Excitability changes in afferent fibre terminations and their relahon to slow potentials. J. Ph~~iol. 142: l-21.
INTRAGENICULATE TERMINAL DEPOLARIZATION THE CAT’S RETINAL GANGLION CELL AXONS DURING RESERPINE-INDUCED PGO-SPIKE
OF
T. SATOH,N. KANAMORI and L. M. VERNON Department of Physiology. School of Dentistry, Aichi-Gakuin University, Nagoya. 464, Japan
(Accepted I Jlrrle 1974)
Summary-Intrageniculate terminal depolarization of the retinal ganglion cell axons is enhanced during the occurrence of reserpine-induced ponto-geniculo-occipital-spikes (PGOK) in the cat immobilized with gallamine triethiodide, thus providing additional evidence for the functional similarity of PGO, to PGO-spikes occurring during REM sleep and arousal. It is suggested that during PGOa, one of the essential changes occurring in the lateral geniculate body is an alteration of the interaction between different retinal afferents.
Erratic field potential changes occurring synchronously with rapid eye movements have been recorded in a variety of brain areas involved in oculomotor and visual functions (JOUVET, 1969). According to the sites of their main occurrence, these potentials are generally called ponto-geniculo-occipital (PGO) spikes. As to the physiological significance of these spikes, feed-forward control of the oculomotor centre over the visual system has been hypothesized. In support of this idea, terminal depolarization of the retinal ganglion cell axons occurs synchronously with PGO-spikes during rapid eye movement (REM) sleep of the cat (IWAMA,KAWAMOTO, SAKAKURA and KASAMATSU,1966) and during saccadic eye movements of the awake monkey (FELDMAN and COHEN, 1968); thus suggesting presynaptic inhibition of the visual input during rapid eye movements. On the other hand, spike activity apparently similar to PGO-spikes of REM sleep and of arousal has been found in reserpine-treated cats (DELORME, JEANNEROD and JOUVET, 1965). Recent investigations have revealed that the reserpine-induced PGO-spike (PGOR) possesses several functional characteristics quite close to those of PGO-spikes found on other backgrounds (BROOKSand GERSHON, 1971; MUNSON and GRAHAM, 1971; SATOH, 1972).
The present investigation was undertaken to find out whether, during PGO,, there are changes at the retinal ganglion cell terminals, which are comparable to those observed during PGO-spikes of REM sleep and arousal. Cats were operated under ether anaesthesia. Reserpine, @5 mg/kg (Apoplon. Dai-ichi Seiyaku) was administered intravenously at least 3 hr before the start of the recording. After interruption of ether, the animal was immobilized with gallamine triethiodide (Teikoku Chemical) and submitted to artificial respiration. Pressure points and wounds were heavily infiltrated with long-lasting procaine chloride jelly. The rectal temperature was
i191
1192
T.
SATOH,
N.
KANAMOKIand L. M. V~KNON
maintained at 375°C. Rectangular pulses of 0.01 msec duration were delivered every 1 set through stimulating electrodes in the lateral geniculate body (LGB). Antidromically elicited compound action potentials were picked up monopolarly from the ipsilateral optic tract about 1 mm caudal to the optic chiasm. The reserpine-induced PGO spike was obtained bipolarly from the contralateral LGB.
LGB
OT
Fig. 1. Enhancement of amplitude of antidromic compound action potential during PGO, (right arrow) relative to control response (left arrow). UT; optic tract response to electrical stimulation of the ipsilateral LGB.
The responses obtained from the optic tract had l-3 peaks. The response with peak latency at about 0.8 msec could be most stably recorded. so the analysis was confined to that wave. Effect
of reserpne
- PGO upon
ant ldromic
response
32
L
RdR
5”
mz
Fig. 2. On the right, total number ofexperiments in which the enhancement ofantidromic response during PGOR was significant (hatched column) or non-significant (open column) at the level P < 0.05 (Student’s t-test). The number of measured responses associated or unassociated with PGOn was 35-85 (mostly 5C-60) in each experiment. The abscissa is the average degrees of increase in the optic tract response during PGO,.
When the test stimulus was given to the LGB during the occurrence of PGO,,, the amplitude of the optic tract response was increased in most occasions (Fig. 1). A summary of sites in the results obtained from 11 cats is found in Figure 2. Among the 46 stimulated the LGB, 32 gave an increase in response size during PGO,. The degree of increase varied considerably from experiment to experiment. This degree is dependent not only on the number of fibres receiving terminal depolarization, but also on the number of fibres which were stimulated at their axon stems, instead of the axon terminals. However, there was
Reserpine
PGO-spike
1193
a case in which the increase reached 40 per cent; indicating that the fibres undergoing an enhanced terminal depolarization during PGO, are fairly numerous. There were some experiments in which the response did not show any significant change during PGOK. In these experiments, a theoretical possibility is that the responses were produced mainly by stimulating the intrageniculate axon stems of the retinal ganglion cells. The present results show that the intrageniculate terminals of retinal ganglion cell axons are depolarized during PGO,. It follows that the functional role of PGO, in the LGB is quite similar to that of PGO-spikes during REM sleep and arousal. This is consistent with the data hitherto obtained that those three kinds of PGO-spikes possess many properties in common. SINCZII (1973) has observed terminal depolarization of retinal ganglion cell axons during PGO-like slow waves elicited by electrical stimulation of the mesencephalic reticular formation. He has concluded that the presence of presynaptic inhibition is questionable, since the transmission of the optic nerve impulses through the LGB was not impaired significantly during those waves. His conclusion raises a serious question about the physiological significance of the ganglion cell axon terminal depolarization which has been repeatedly observed in different experimental situations. However, detection of terminal depolarization by the excitability testing method of WALL (1958) does not prove conclusively that it is those fibres synapsing onto the principal cells of the LGB which are depolarized. If the depolarization were operating at axon branch terminals which are connected to LGB internuncial neurones not directly involved in the transmission of visual information to the visual cortex. it would be possible to obtain an enhanced antidromic response simultaneously with unimpaired transmission from the optic tract to the optic radiation. Furthermore, in view of the fact that the internuncial neurones are mostly inhibitory to the principal cells, the diminished excitation of the former during PGO,< would result in disinhibition of the latter, the occurrence of which has been deduced from the results of stimulation of the mesencephalic reticular formation (FUKLDA and IWAMA, 1971; SINGER, 1973). Therefore, it seems that during PGO, one of the essential changes occurring in the LGB would be an altered interaction between different retinal affercnts. rather than reduced transmission of visual information. REFERENCES BKOOKS, D. C. and &RSNOh, M. D. (1971). Eye movement potentials in the oculomotor and visual systems of the cat: a comparison of reserpine induced waves with those present during wakefulness and rapid eye movement sleep. Brain Rcs. 21: 223-239. DIXORME, F., JIIANNFROD.M. and JOYVET. M. (1965). Effets remarquables de la riserpine sur l’activite EEG phasique ponto-g&niculo-occipitale. C. I’. Siarlc. Sec. Biol. 15% 90@903. FELLNAN’, M. and COHEN. B. (1968). Electrical activity in the lateral geniculate body of the alert monkey associated with eye movements. J. Nrz~opl~~siol. 31: 455-466. FCKUUA. Y. and IWAMA, K. (1971). Reticular inhibition of internuncial cells in the rat lateral geniculate body. Brait] Rrs. 35: 107-l 18. IWAMA. K.. KAWAMOTO. T.. SAKAKURA, H. and KASAMATSU.T. (1966). Responsiveness of cat lateral geniculate at pre- and postsynaptic levels during natural sleep. Physiol. Behao. I: 45-53. JOIVIZ~, M. (1969). Biogenic amines and the states of sleep. Science. N.Y 163: 32-41. MUNSON. J. B. and GRAHAM. R. B. (1971). Lateral geniculate spikes in sleeping. awake, and reserpine-treated cats: correlated excitability changes in superior colliculus and related structures. EvpI Nru,ol. 31: 326-336. SATOH. T. (1972). Cortical responsiveness during reserpine-induced PGO-spike in the cat. lnt. J. Neurosci. 3: 201204. SINXR. W. (1973). Brain stem stimulation and the hypothesis of presynaptic inhibition in cat lateral geniculate nucleus. Bruin Res. 61: 55-68. WALL. P. D. (1958). Excitability changes in afferent fibre terminations and their relahon to slow potentials. J. Ph~~iol. 142: l-21.