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Fast conducting electrosensory pathway in the mormyrid fish, Gnathonemus petersii
Neuroscience Letters, 2 (1976) 133--136 © Elsevier/North-Holland, Amsterdam -- Printed in The Netherlands
133
FAST CONDUCTING E L E C T R O S E N S O R Y PATHWAY IN THE MORMYRID FISH, GNATHONEMUS PETERSII
P.S. ENGER*, S. LIBOUBAN and T. SZABO
Laboratoire de Physiologie Nerveuse, D~parternent de Neurophysiologie Sensorielle, CNRS, 91190 Gif sur Yvette (France) (Received March 5th, 1976) (Accepted March 31st, 1976)
SUMMARY
A c o m p o u n d action potential of short latency was recorded from the ganglion mesencephali extrolaterale in response to b o t h the fish's o w n electric organ discharge and electric stimulation of the whole fish or a branch of the posterior lateral line nerve. The time difference between the response in the nerve, 16 mm from its entry into the brain, and the mesencephalic ganglion, which is positioned 10 mm anterior in the CNS, was f o u n d to be 1.6 msec. This rapid conduction pathway involves peripheral nerve fibres of high conduction velocity (40 m/sec) and presumably t w o electric synapses, one at the rhombencephalic and the other at the mesencephalic level.
In all gymnotids so far examined, the fish's own electric organ discharge (EOD) provokes a short latency response in a particular part of the mesencephalon. The response is due to the activation of the fast conducting and electrotonically coupled pathway previously described in the electrosensory system of these fish [ 4,6]. Bennett and Steinbach [ 1 ], working on curarized 'Gnathonemus petersii, also reported that an extrinsic electric stimulus evokes a similar response in the midbrain of this species, which belongs to the other weakly electric fish family, the Mormyridae. The purpose of the present study was to investigate electrophysiologically this rapid pathway in Gnathonemus petersii, particularly with respect to the morphological findings of Szabo and Ravaille [5]. The fish was anaesthetized with MS 222, wrapped in gauze and placed in a normal upright position in a small container by pinning the gauze to a paraffin board. Only the dorsal part of the head was above the water surface and the fish was fitted with a glass m o u t h piece through which water or a weak MS 222 solution was supplied. The brain was exposed and 150 ~m *On sabbatical leave from the University of Oslo, Oslo 3, Norway.
134 steel electrodes or 10--15 pm glass pipettes filled with 3 M NaC1 were placed on the ganglion mesencephali extrolaterale (g.mes.extrolat.) and in the nucleus lobi lineae lateralis (nLLL), respectively. The g.mes.extrolat, was reached by gently displacing the overlying cerebellum to one side, and the electrode was placed on the surface under visual control. Responses were obtained only from the anterior part of the ganglion. This area, consisting of a neuropile with relatively few cell bodies (Fig. 1) [6], had a high background level of nervous activity.
Fig. 1. Cross-section of the brain at the level of ganglion mesencephali extrolaterale • (g.mes.ext.lat.). Note neuropile in the ganglion. 11, lemniscus lateralis; g.mes.lat, and ext.lat., ganglion mesencephali laterale et extrolaterale; v~lv.cereb, valvula cerebelli; tect.opt., tecturn opticurn. The second electrode was lowered at a 45 ° angle through the cerebellum and lobus caudalis into the nLLL. The recording site was coagulated for histological control. The fish was stimulated either by weak electrical stimulation, applied through small silver plates placed in front of and behind the fish, or by its own EOD. The response in g.mes.extrolat, consisted of a c o m p o u n d action potential with a refractory period of about 3 msec of which the absolute refractory period was less than I msec. The peak latency of the response was around 3 msec, ranging from 2.9 to 3.2 msec in 9 experiments and a latency of the initial phase some 0.5 msec shorter (Fig. 2A). (In one experiment the peak
135
B
A
dZ~
0
ILl
I
g m e s ext-lat
1
;
c
?
,
~1
I
i i t
nLLL
] 02mY[
L
I
Fig. 2. A: responses in nLLL (upper trace in each record) and g.mes.ext.-lat. (lower trace) to electric organ discharge (EOD) and to submaximal and maximal electrical stimulation. B: display of latency differences of responses to electrical stimulation of the whole fish. Recording sites indicated on the figure. LLLp, posterior branch of the lateral line nerve. Vertical bar: 0.2 inV. latency was 3.8 msec). Almost half o f the latency time can be a c c o u n t e d for by stimulation o f t he electroreceptors plus c o n d u c t i o n of impulses in the peripheral nerves. This is illustrated in Fig. 2B which shows records of 'activity in g.mes.extrolat, and in strands of nerve fibres in the dorsal branch of the lateral line nerve during electric field stimulation of the fish. T he time difference b etween t he responses in the nerve and in t he mesencephalon is 1.6 msec. A latency of 1.6 msec was also f o u n d for the mesencephalic response when stimulating t he nerve at the same place. The conducting distance f r o m th e site of the stimulating electrodes t o t he n L L L is 16--18 mm, and a b o u t a n o t h e r 10 m m t o the g.mes.extrolat. The c o n d u c t i o n velocity in t h e dorsal nerve has been measured and f o u n d to be 40 m/sec. The c o n d u c t i o n velocity of the central axons is n o t known, b ut f r o m anatomical data [5] an estimate o f 15 m/sec seems reasonable -- giving 0.7 msec for central impulse propagation. This leaves 0.5 msec for the transmission time at the t w o probable synapses. The first one is presumably in the n L L L [ 2 ] . The response in this nucleus precedes th at in the g.mes.extrolat, by only 1.0 msec (Fig. 2B). The responses in n L L L and g.mes.extrolat, follow each o t h e r closely in amplitude when the
~36
strength of the electrical stimulation is varied (Fig. 2A). The maximal responses as well as the just noticeable response, are obtained at the same stimulus intensity in both loci. This indicates the presence of a direct connection between the two loci. The g.mes.extrolat, is the location of the second synapse. This conclusion is based on the observation of the response latency as the electrode is lowered from the surface towards the fibre tract connecting the nLLL and g.mes.extrolat. (Fig. 1). At a level at which no cell bodies are located (i.e., medial and ventral to the ganglion}, the peak latency of the response becomes about 0.3 msec shorter. The present findings confirm the existence of a rapid electrosensory pathway in the mormyrid fish, G n a t h o n e r n u s p e t e r s i i , similar to that already described in gymnotids [4]. As supported by anatomical data [ 5,6], the short latency response evoked in the mesencephalon by electric field stimulation {artificial or natural EOD) of the fish is relayed at the rhombencephalic level in t h e nLLL. This conclusion is also confirmed by the presence of stained cells in the nLLL after injection of horseradish peroxidase in the g.mes.extrolat. Displaying a short refractory period, the nLLL (in accordance with Bell, personal communication) and the mesencephalic response tolerate high frequency stimulation. This physiological property also confirms the similarity between mormyrid and gymnotid rapid electrosensory pathways. Particular attention should be paid to the fact that, as in gymnotids [3], the fish's o w n E O D evokes a mesencephalic as w e l l as a nLLL response. This contradicts the prediction of Bennett and Steinbach [1], according to which the mesencephalic response does not appear if the external stimulus is delivered within a certain time interval relative to the medullary discharge signal. These authors suggest that an intrinsic feedback, connected to and/or controlled by the fish's EOD command centre, interacts with the incoming electrosensory impulses of the lateral line lobe level and abolishes the mesencephalic responses. The use of curare by these authors might explain this discrepancy between their results and ours. REFERENCES 1 Bennett, M.V.L. and Steinbach, A.B., Influence of electric organ control system on electrosensory afferent pathways in Mormyrids. In R. Llin~ts (Ed.) Neurobiology of Cerebellar Evolution and Development, Amer. Med. Assoc., 1969, pp. 207--214. 2 Maler, L., Karten, H.J. and Bennett, M.V.L., The central connections of the posterior lateral line nerve of Gnathonemus petersiL J. comp. Neurol., 151 (1973) 57--66. 3 Szabo, T., Activity of peripheral and central neurons involved in electroreceptors. In Lateral Line Detectors, 1967, pp. 295--311. 4 Szabo, T., Central processing of messages from tuberous electroreceptors in Teleosts. In A. Fessard (Ed.), Electroreceptors and other Specialized Receptors in Lower Vertebrates, Handbook of Sensory Physiology, III/3, Springer, Berlin, 1974, pp. 95--124. 5 Szabo, T. and Ravaille, M., Synaptic structure of the lateral line lobe nucleus in Mormyrid fish, Neuroscience Letters, 2 (1976) 127--131. 6 Szabo, T., Sakata, H. and Ravaille, M., An electrotonic coupled pathway in the central neuron system of some teleost fish, Gymnotidae and Mormyridae, Brain Res., 95 (1975) 459--474.
133
FAST CONDUCTING E L E C T R O S E N S O R Y PATHWAY IN THE MORMYRID FISH, GNATHONEMUS PETERSII
P.S. ENGER*, S. LIBOUBAN and T. SZABO
Laboratoire de Physiologie Nerveuse, D~parternent de Neurophysiologie Sensorielle, CNRS, 91190 Gif sur Yvette (France) (Received March 5th, 1976) (Accepted March 31st, 1976)
SUMMARY
A c o m p o u n d action potential of short latency was recorded from the ganglion mesencephali extrolaterale in response to b o t h the fish's o w n electric organ discharge and electric stimulation of the whole fish or a branch of the posterior lateral line nerve. The time difference between the response in the nerve, 16 mm from its entry into the brain, and the mesencephalic ganglion, which is positioned 10 mm anterior in the CNS, was f o u n d to be 1.6 msec. This rapid conduction pathway involves peripheral nerve fibres of high conduction velocity (40 m/sec) and presumably t w o electric synapses, one at the rhombencephalic and the other at the mesencephalic level.
In all gymnotids so far examined, the fish's own electric organ discharge (EOD) provokes a short latency response in a particular part of the mesencephalon. The response is due to the activation of the fast conducting and electrotonically coupled pathway previously described in the electrosensory system of these fish [ 4,6]. Bennett and Steinbach [ 1 ], working on curarized 'Gnathonemus petersii, also reported that an extrinsic electric stimulus evokes a similar response in the midbrain of this species, which belongs to the other weakly electric fish family, the Mormyridae. The purpose of the present study was to investigate electrophysiologically this rapid pathway in Gnathonemus petersii, particularly with respect to the morphological findings of Szabo and Ravaille [5]. The fish was anaesthetized with MS 222, wrapped in gauze and placed in a normal upright position in a small container by pinning the gauze to a paraffin board. Only the dorsal part of the head was above the water surface and the fish was fitted with a glass m o u t h piece through which water or a weak MS 222 solution was supplied. The brain was exposed and 150 ~m *On sabbatical leave from the University of Oslo, Oslo 3, Norway.
134 steel electrodes or 10--15 pm glass pipettes filled with 3 M NaC1 were placed on the ganglion mesencephali extrolaterale (g.mes.extrolat.) and in the nucleus lobi lineae lateralis (nLLL), respectively. The g.mes.extrolat, was reached by gently displacing the overlying cerebellum to one side, and the electrode was placed on the surface under visual control. Responses were obtained only from the anterior part of the ganglion. This area, consisting of a neuropile with relatively few cell bodies (Fig. 1) [6], had a high background level of nervous activity.
Fig. 1. Cross-section of the brain at the level of ganglion mesencephali extrolaterale • (g.mes.ext.lat.). Note neuropile in the ganglion. 11, lemniscus lateralis; g.mes.lat, and ext.lat., ganglion mesencephali laterale et extrolaterale; v~lv.cereb, valvula cerebelli; tect.opt., tecturn opticurn. The second electrode was lowered at a 45 ° angle through the cerebellum and lobus caudalis into the nLLL. The recording site was coagulated for histological control. The fish was stimulated either by weak electrical stimulation, applied through small silver plates placed in front of and behind the fish, or by its own EOD. The response in g.mes.extrolat, consisted of a c o m p o u n d action potential with a refractory period of about 3 msec of which the absolute refractory period was less than I msec. The peak latency of the response was around 3 msec, ranging from 2.9 to 3.2 msec in 9 experiments and a latency of the initial phase some 0.5 msec shorter (Fig. 2A). (In one experiment the peak
135
B
A
dZ~
0
ILl
I
g m e s ext-lat
1
;
c
?
,
~1
I
i i t
nLLL
] 02mY[
L
I
Fig. 2. A: responses in nLLL (upper trace in each record) and g.mes.ext.-lat. (lower trace) to electric organ discharge (EOD) and to submaximal and maximal electrical stimulation. B: display of latency differences of responses to electrical stimulation of the whole fish. Recording sites indicated on the figure. LLLp, posterior branch of the lateral line nerve. Vertical bar: 0.2 inV. latency was 3.8 msec). Almost half o f the latency time can be a c c o u n t e d for by stimulation o f t he electroreceptors plus c o n d u c t i o n of impulses in the peripheral nerves. This is illustrated in Fig. 2B which shows records of 'activity in g.mes.extrolat, and in strands of nerve fibres in the dorsal branch of the lateral line nerve during electric field stimulation of the fish. T he time difference b etween t he responses in the nerve and in t he mesencephalon is 1.6 msec. A latency of 1.6 msec was also f o u n d for the mesencephalic response when stimulating t he nerve at the same place. The conducting distance f r o m th e site of the stimulating electrodes t o t he n L L L is 16--18 mm, and a b o u t a n o t h e r 10 m m t o the g.mes.extrolat. The c o n d u c t i o n velocity in t h e dorsal nerve has been measured and f o u n d to be 40 m/sec. The c o n d u c t i o n velocity of the central axons is n o t known, b ut f r o m anatomical data [5] an estimate o f 15 m/sec seems reasonable -- giving 0.7 msec for central impulse propagation. This leaves 0.5 msec for the transmission time at the t w o probable synapses. The first one is presumably in the n L L L [ 2 ] . The response in this nucleus precedes th at in the g.mes.extrolat, by only 1.0 msec (Fig. 2B). The responses in n L L L and g.mes.extrolat, follow each o t h e r closely in amplitude when the
~36
strength of the electrical stimulation is varied (Fig. 2A). The maximal responses as well as the just noticeable response, are obtained at the same stimulus intensity in both loci. This indicates the presence of a direct connection between the two loci. The g.mes.extrolat, is the location of the second synapse. This conclusion is based on the observation of the response latency as the electrode is lowered from the surface towards the fibre tract connecting the nLLL and g.mes.extrolat. (Fig. 1). At a level at which no cell bodies are located (i.e., medial and ventral to the ganglion}, the peak latency of the response becomes about 0.3 msec shorter. The present findings confirm the existence of a rapid electrosensory pathway in the mormyrid fish, G n a t h o n e r n u s p e t e r s i i , similar to that already described in gymnotids [4]. As supported by anatomical data [ 5,6], the short latency response evoked in the mesencephalon by electric field stimulation {artificial or natural EOD) of the fish is relayed at the rhombencephalic level in t h e nLLL. This conclusion is also confirmed by the presence of stained cells in the nLLL after injection of horseradish peroxidase in the g.mes.extrolat. Displaying a short refractory period, the nLLL (in accordance with Bell, personal communication) and the mesencephalic response tolerate high frequency stimulation. This physiological property also confirms the similarity between mormyrid and gymnotid rapid electrosensory pathways. Particular attention should be paid to the fact that, as in gymnotids [3], the fish's o w n E O D evokes a mesencephalic as w e l l as a nLLL response. This contradicts the prediction of Bennett and Steinbach [1], according to which the mesencephalic response does not appear if the external stimulus is delivered within a certain time interval relative to the medullary discharge signal. These authors suggest that an intrinsic feedback, connected to and/or controlled by the fish's EOD command centre, interacts with the incoming electrosensory impulses of the lateral line lobe level and abolishes the mesencephalic responses. The use of curare by these authors might explain this discrepancy between their results and ours. REFERENCES 1 Bennett, M.V.L. and Steinbach, A.B., Influence of electric organ control system on electrosensory afferent pathways in Mormyrids. In R. Llin~ts (Ed.) Neurobiology of Cerebellar Evolution and Development, Amer. Med. Assoc., 1969, pp. 207--214. 2 Maler, L., Karten, H.J. and Bennett, M.V.L., The central connections of the posterior lateral line nerve of Gnathonemus petersiL J. comp. Neurol., 151 (1973) 57--66. 3 Szabo, T., Activity of peripheral and central neurons involved in electroreceptors. In Lateral Line Detectors, 1967, pp. 295--311. 4 Szabo, T., Central processing of messages from tuberous electroreceptors in Teleosts. In A. Fessard (Ed.), Electroreceptors and other Specialized Receptors in Lower Vertebrates, Handbook of Sensory Physiology, III/3, Springer, Berlin, 1974, pp. 95--124. 5 Szabo, T. and Ravaille, M., Synaptic structure of the lateral line lobe nucleus in Mormyrid fish, Neuroscience Letters, 2 (1976) 127--131. 6 Szabo, T., Sakata, H. and Ravaille, M., An electrotonic coupled pathway in the central neuron system of some teleost fish, Gymnotidae and Mormyridae, Brain Res., 95 (1975) 459--474.