Abstract
-
1.
Response properties of neurons in the dorsal granular ridge (DGR) of the little skate, Raja erinacea, were studied in decerebrate, curarized fish. Sensory responses included proprioceptive (426 of 952; 45%) and electroreceptive units (526 of 952; 55%). Electroreceptive units responded to weak electric fields with a higher threshold than lower-order units and had large ipsilateral receptive fields, whose exact boundaries were often unclear but contained smaller, identifiable best areas. Proprioceptive units responded to displacement of the ipsilateral fin and were either position-or movement-sensitive.
-
2.
Both proprioceptive and electroreceptive units showed a progression of receptive fields from anterior to posterior body in the rostral to caudal direction along the length of DGR. Sensory maps in DGR projected homotopically to the electrosensory somatotopy in the dorsal nucleus. Peak evoked potentials and units responding to local DGR stimulation occurred only in areas of the dorsal nucleus with receptive fields located within the composite receptive field at the DGR stimulation site.
-
3.
Single shocks to DGR produced a short spike train followed by a prolonged suppression period in the medullary dorsal nucleus. These results have implications for the role of the parallel fiber system in medullary electrosensory processing.
Similar content being viewed by others
Abbreviations
- AEN:
-
ascending efferent neuron
- DGR:
-
dorsal granular ridge
- EPSP:
-
excitatory postsynaptic potential
- IPSP:
-
inhibitory postsynaptic potential
- IR:
-
intensity-response
- LG:
-
lateral granular area
- LMN:
-
lateral mesencephalic nucleus
- S:N:
-
signal to noise ratio
- TTL:
-
transistor-transistor logic
References
Bastian J (1982) Vision and electroreception: integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. J Comp Physiol 147:287–297
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 158:505–515
Bastian J, Courtright J (1991) Morphological correlates of pyramidal cell adaptation rate in the electrosensory lateral line lobe of weakly electric fish. J Comp Physiol A 168:393–407
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, Montgomery JC (1992) Suppression of ventilatory reafference in the elasmobranch electrosensory system: medullary neuron receptive fields support a common mode rejection mechanism. J Exp Biol 171:127–137
Bodznick D, Schmidt AW (1984) Somatotopy within the medullary electrosensory nucleus of the little skate, Raja erinacea. J Comp Neurol 225:581–590
Bodznick D, Montgomery JC, Bradley DJ (1992) Suppression of common mode signals within the electrosensory system of the little skate Raja erinacea. J Exp Biol 171:107–125
Conley RA (1991) Electro receptive and proprioceptive representations in the dorsal granular ridge of skates. Ph. D. thesis, Wesleyan University, Middletown
Crowe A, Matthews PBC (1964a) The effects of stimulation of static and dynamic fusimotor fibres on the response to stretching of the primary endings of muscle spindles. J Physiol (Lond) 174:109–131
Crowe A, Matthews PBC (1964b) Further studies of static and dynamic fusimotor fibres. J Physiol (Lond) 174:132–151
Eccles JC, Ito M, Szentagothai J (1967) The cerebellum as a neuronal machine. Springer, Berlin Heidelberg New York
Fessard A, Sand A (1937) Stretch receptors in the muscles of fishes. J Exp Biol 14:382
Granit R, Phillips CG (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J Physiol (Lond) 133:520–547
Kalmijn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A (ed) Handbook of sensory physiology, vol III/3. Springer, Berlin Heidelberg New York, pp 147–200
Kalmijn AJ (1988) Detection of weak electric fields. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 151–185
Llinás R, Nicholson C (1971) Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol 34:532–551
Loewenstein WR (1960) Mechanisms of nerve impulse initiation in a pressure receptor (Lorenzinian ampulla). Nature 122:1034
Montgomery JC (1984a) Frequency response characteristics of primary and secondary neurons in the electrosensory system of the thornback ray. Comp Biochem Physiol A 79:189–195
Montgomery JC (1984b) Noise cancellation in the electrosensory system of the thornback ray; common mode rejection of input produced by the animal's own ventilatory movement. J Comp Physiol A 155:103–111
Montgomery JC, Bodznick D (1994) Hindbrain circuitry mediating common mode suppression of ventilatory reafference in the electrosensory system of the little skate, Raja erinacea. J Exp Biol 183:203–215
Murray RW (1960) The response of ampullae of Lorenzini of elasmobranchs to mechanical stimulation. J Exp Biol 37:417–424
Murray RW (1965) Electroreceptor mechanism: The relationship of stimuli in the ampullae of Lorenzini of elasmobranchs. In: Cahn P (ed) Lateral line detectors. Univ of Indiana, Bloomington, pp 277–452
New JG (1986) Sensory processing in the medullary electrosensory nucleus of the little skate, Raja erinacea. Ph D dissertation, Wesleyan University, Middletown
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
Nicholson C, Llinás R (1969) Inhibition of Purkinje cells in the cerebellum of elasmobranch fishes. Brain Res 12:477–480
Nicholson C, Llinás R, Precht W (1969) Neural elements of the cerebellum in elasmobranch fishes: Structural and functional characteristics. In: Llinás E(ed) Neurobiology of cerebellar evolution and development. American Medical Association, Chicago, pp 215–244
Paul DH, Roberts BL (1977) Studies on primitive cerebellar cortex. I. Anatomy of lateral line lobes of dogfish, Scyliorhinus canicula. Proc R Soc (Lond) B 195:435–466
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
Schweitzer J (1983) The physiological and anatomical localization of two electroreceptive and diencephalic nuclei in the thornback ray, Platyrhinoidis triseriata. J Comp Physiol 153:331–341
Schweitzer J (1986) Functional organization of the electroreceptive midbrain in an elasmobranch (Platyrhinoidis triseriata). J Comp Physiol A 158:43–58
Skarf B, Jones ML (1981) Vestibular-visual interactions in frog mesencephalon during natural stimulation. Brain Res 206:457–461
Sperry DG, Boord RL (1992) Central location of the motoneurons that supply the cucullaris (trapezius) of the clearnose skate, Raja eglanteria. Brain Res 582:312–319
Terashima S, Goris RC (1975) Tectal organization of pit viper infrared reception. Brain Res 83:490–494
Welker W (1987) Spatial organization of somatosensory projections to granule cell cerebellar cortex: functional and connectional implications of fractured somatotopy. In: King (ed) New concepts in cerebellar neurobiology. Liss, New York, pp 239–280
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Conley, R.A., Bodznick, D. 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 (1994). https://doi.org/10.1007/BF00192720
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00192720