Abstract
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1.
The dorsal octavolateralis nucleus is the primary electrosensory nucleus in elasmobranchs and receives a major descending input from the dorsal granular ridge (DGR), a part of the vestibulolateral cerebellum. Removal of DGR altered the response properties of ascending efferent neurons (AENs), the projection neurons of the dorsal octavolateralis nucleus.
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2.
Elimination of DGR by lesion or lidocaine microinjection increased the excitability in AENs. Spontaneous activity increased by 680% and receptive fields became 1300% larger. The sensitivity of AENs to electric field stimuli increased by 560% and the time constant of adaptation increased by 300%, while threshold sensitivity remained unchanged.
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3.
Some electrosensory units responded to proprioceptive stimuli. In intact animals, the spontaneous activity of AENs was much less modulated by changes in fin position than primary electroreceptor afferents. Lesions to DGR appeared to increase the responsiveness of AENs to changes in fin position.
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4.
These results indicate that the action of DGR on the dorsal octavolateralis nucleus is primarily inhibitory and may function in a gain control mechanism. The possibility also exists for a mechanical-reafferent reduction mechanism in the electrosensory system of the elasmobranch that may be mediated by DGR.
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References
Bass AH (1982) Evolution of the vestibulolateral lobe of the cerebellum in electroreceptive and non-electroreceptive teleosts. J Morphol 174:335–348
Bastian J (1981a) An analysis of the effects of moving objects and other electrical stimuli on the electroreceptor activity of Apteronotus albifrons. J Comp Physiol 144:465–479
Bastian J (1981b) Electrolocation II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J Comp Physiol 144:481–494
Bastian J (1986a) Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6(2):553–562
Bastian J (1986b) Gain control in the electrosensory system: A role for descending projections to the electrosensory lateral line lobe. J Comp Physiol A 158:332–337
Bastian J (1993) Proprioceptive and electroreceptive inputs to the gymnotiform electrosensory system are modulated by changes in body geometry. Soc Neurosci Abstr 19:375
Bastian J (1994) Descending control and the physiology of the electrosensory lateral line lobe in gymnotid fish. Assoc Res Otolaryngol Abstr 17:621
Bodznick D, Boord RL (1986) Electroreception in Chondrichthyes: Central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 225–256
Bodznick D, Schmidt AW (1982) Functional connections of the medullary electroreceptor nucleus of the skate. Soc Neurosci Abstr 8:763
Boord RL, Northcutt RG (1982) Ascending lateral line pathways to the midbrain of the clearnose skate, Raja eleganteria. J Comp Neurol 207:274–282
Bratton BO, Ayers JL (1987) Observations on the electric organ discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behaviour. Environmental Biology of Fishes 20:241–254
Bratton BO, Christiano A, McClennen N, Murray M, O'Neill E, Ritzen K (1993) The electric organ discharge of the skate (Rajidae) waveform, occurrence and behavior relationships. Soc Neurosci Abstr 19:374
Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive sense modality. Brain Res Rev 6:25–46
Conley R (1991) Electroreceptive and proprioceptive representations in the dorsal granular ridge of skates. Ph. D. Thesis, Wesleyan University
Conley R, Bodznick D (1994) The cerebellar dorsal granular ridge in an elasmobranch has proprioceptive and electroreceptive representations and projects homotopically to the medullary electrosensory nucleus. J Comp Physiol A 174:707–721
Hjelmstad GO, Parks G, Bodznick D (1993) A corollary discharge of the ventilatory motor command in the dorsal granular ridge of skates; implications for electrosensory processing. Soc Neurosci Abstr 19:374
Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191
Lissmann HW, Machin KE (1958) The mechanism of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35:451–486
Lowenstein W (1960) Mechanisms of nerve impulse initialization in a pressure receptor (Lorenzinian ampulla). Nature 122:1034
Maler L (1973) The posterior lateral line lobe of a mormyrid fish — A Golgi study. J Comp Neurol 152:281–298
Maler L (1974) The acousticolateral area of bony fishes and its cerebellar relations. Brain Behav Ecol 10:130–145
McCormick CA (1982) The organization of the octavolateralis area in actinoptergian fishes: a new interpretation. J Morphol 171:159–181
Mikhailenko NA (1971) Biological significance and dynamics of electrical discharges in weak electrical fishes of the Black Sea. Zool Zh 50:1347–1352
Montgomery JC (1984) Frequency response characteristics of primary and secondary neurons in the electrosensory system of the thornback ray. Comp Biochem Physiol A 79:189–195
Murray RW (1960) The response of ampullae of Lorenzini of elasmobranchs to mechanical stimulation. J Exp Biol 37:417–424
New JG (1989) Sensory processing in the medullary electrosensory nucleus of the little skate, Raja erinacea. Ph D Dissertation, Wesleyan University
New JG (1989) Electric organ discharge and electrosensory reafference in the little skate, Raja erinacea. Biol Bull 177:32
New JG (1990) Medullary electrosensory processing in the little skate. I. Response characteristics of neurons in the dorsal octavolateralis nucleus. J Comp Physiol A 167:285–294
New JG, Bodznick D (1990) Medullary electrosensory processing in the little skate. II. Suppression of self-generated electrosensory interference during respiration. J Comp Physiol A 167:295–307
Paul DH, Roberts BL (1977) Studies on a primitive cerebellar cortex. I. The anatomy of the lateral-line lobes of the dogfish, Scyliorhinus canicula. Proc R Soc Lond B 195:453–466
Paul DH, Roberts BL, Ryan KP (1977) Comparison between lateral-line lobes of the dogfish and the cerebellum: An ultrastructural study. J Hirnforsch 18:335–343
Salyapongse A, Hjelmstad G, Bodznick D (1992) Second-order electroreceptive cells in skates have response properties dependent on the configuration of their inhibitory receptive fields. Biol Bull 183:349
Schmidt AW, Bodznick D (1987) Afferent and efferent connections of the vestibulolateral cerebellum of the little skate, Raja erinacea. Brain Behav Evol 30:282–302
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Conley, R.A. Descending input from the vestibulolateral cerebellum suppresses electrosensory responses in the dorsal octavolateralis nucleus of the elasmobranch, Raja erinacea . J Comp Physiol A 176, 325–335 (1995). https://doi.org/10.1007/BF00219058
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DOI: https://doi.org/10.1007/BF00219058