The Laminar organization of optic nerve fibres in the tectum of goldfish

Potentials in the tectum of large (12─20 cm) goldfish, evoked by stimulation of the optic nerve, were recorded extracellularly with double-barrelled electrodes (d. c., saline and a. c., Woods metal─Pt). Four fibre groups (E, M1, M2, M3) were recorded at latencies of approximately 2, 3, 5 and 8 ms after stimulation (conduction velocities of approximately 7, 5, 3 and 2 m/s). The same four groups were recorded from the optic nerve when the tectum was stimulated. The fastest fibre group (E) did not give rise to a postsynaptic wave. Fibre groups M1, M2 and M3 gave rise to postsynaptic potentials which, following computation of their second spatial derivatives with depth, were found to have current sinks at depths of approximately 100─50 μm, 150─200 μm and 250-350 μm respectively. Thus the fastest conducting retinotectal fibres make their synapses most superficially, the opposite of the arrangement in the frog tectum. These postsynaptic waves fatigued at repetitive stimulus rates of 20─50 per second, and in twin pulses at interstimulus intervals of 10─15 ms; and they were reversibly blocked by topical application of pentobarbitol. The fibre potentials, however, were virtually undecremented under these conditions. To compare these electrophysiological findings with the anatomy, the cobalt procedure was used to visualize the profiles of the optic fibres in the various tectal laminae. A thick dense projection filled the superficial grey and white (s. g. w.) layer, and there was a thin satellite band just superficial to it. In addition, there were two deeper bands of sparse innervation, in the middle of the central grey zone (c. g.) and in the deep white (d. w.) layer. These bands were associated with the field potential sinks through lesions made with recording electrodes. The two deep bands correspond to the M3 fibre group. The dense s. g. w. innervation contains both the M1 and M2 fibre groups, the M1 just superficial to the M2. The fastest fibre group, E, which had no postsynaptic wave associated with it, persisted at least six weeks after retinal removal, and probably represents efferent cells with fibres projecting back through the optic nerve to the retina. Filled cell profiles could not be positively identified with the cobalt technique, but could be seen with the HRP technique, when the optic afferents were first allowed to degenerate. The filled cells were the pyramidals of the s. g. w. layer.

[1]  R. Nicoll Pentobarbital: differential postsynaptic actions on sympathetic ganglion cells. , 1978, Science.

[2]  C. Weidner,et al.  An experimental study of the visual system of cyprinid fish using the HRP method , 1977, Brain Research.

[3]  N. Schellart,et al.  Shapes of receptive field centers in optic tectum of goldfish , 1976, Vision Research.

[4]  R. M. Gaze,et al.  The arrow model: retinotectal specificity and map formation in the goldfish visual system , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[5]  C. Nicholson,et al.  Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. , 1975, Journal of neurophysiology.

[6]  T. Bliss,et al.  The synaptic organization of optic afferents in the amphibian tectum , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  E. M. Bell,et al.  The intensification of cobalt-filled neurone profiles using a modification of Timm's sulphide-silver method. , 1974, Brain research.

[8]  D. Sandeman,et al.  Efferent axons in the fish optic nerve and their effect on the retinal ganglion cells. , 1974, Brain research.

[9]  G. Shepherd,et al.  Current-density analysis of summed evoked potentials in opossum prepyriform cortex. , 1973, Journal of neurophysiology.

[10]  H. Vanegas,et al.  Electrophysiological evidence of tectal efferents to the fish eye. , 1973, Brain research.

[11]  C. D. Richards On the mechanism of barbiturate anaesthesia , 1972, The Journal of physiology.

[12]  N. Daw,et al.  Unusual units in the goldfish optic nerve. , 1972, Vision research.

[13]  B. Agranoff,et al.  Radioautography of the Optic Tectum of the Goldfish after Intraocular Injection of [3H]Proline , 1972, Science.

[14]  S. Sharma,et al.  The retinal projections in the goldfish: an experimental study. , 1972, Brain research.

[15]  H. Vanegas,et al.  Response of the optic tectum to stimulation of the optic nerve in the teleost Eugerres plumieri. , 1971, Brain research.

[16]  J. Stone,et al.  Synaptic organisation of the pigeon's optic tectum: a golgi and current source-density analysis. , 1971, Brain research.

[17]  G. Y. Sze´kely,et al.  Distribution of optic terminals in the different optic centres of the frog. , 1969 .

[18]  G. Shepherd,et al.  Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. , 1968, Journal of neurophysiology.

[19]  H. Knapp,et al.  New Observations on the Retinal Projection in the Frog , 1968 .

[20]  B. Katz Nerve, Muscle and Synapse , 1966 .

[21]  M. Lemire,et al.  Retinal projections in cyprinid fishes: a degeneration and radioautographic study. , 1976, Brain, behavior and evolution.

[22]  H Spekreijse,et al.  Spectral and spatial coding of ganglion cell responses in goldfish retina. , 1972, Journal of neurophysiology.

[23]  R. Burke,et al.  Electrotonic characteristics of alpha motoneurones of varying size , 1971, The Journal of physiology.

[24]  C. Prosser,et al.  Electrical properties of goldfish optic tectum. , 1970, Journal of neurophysiology.

[25]  R. M. Gaze The formation of nerve connections , 1970 .

[26]  J. Konishi ELECTRIC RESPONSE OF VISUAL CENTER TO OPTIC NERVE STIMULATION IN FISH , 1960 .

[27]  C. S. S.,et al.  The Comparative Anatomy of the Nervous System of Vertebrates, including Man , 1937, Nature.