Functional circuitry of the goldfish cerebellum

The responses of cerebellar units following electrical stimulation applied to the area dorsalis centralis (Dc) of the telencephalon were studied in the siluroid teleost Ictalurus nebulosus. Two kinds of units are distinguished on physiological criteria, identified as Purkinje and eurydendroid cells (the efferent neurons of the cerebellum in teleosts equivalent to cells of the deep nuclei in other vertebrates). A high proportion of both kinds of units in the corpus cerebelli are sensitive to such stimulation. Each kind of unit shows several consistent response types. Purkinje cells fire simple spikes spontaneously at the rate of 8–50 spikes/s and respond to a single shock to Dc with an initial latency of 34–64 ms. The response can be one of the following types: (1) inhibition alone, with a duration of 0.3–1.5 s; (2) initial inhibition for 0.04–0.2 s, followed by postinhibitory rebound, or (3) initial excitation followed by inhibition which may or may not be followed by a late excitation. It is suggested that the initial excitation and initial inhibition reflect the activation of mossy fiber-granule cell-Purkinje cell circuitry and mossy fiber-granule cell-inhibitory interneuron-Purkinje cell circuitry, respectively. Indirect evidence suggests the involvement of climbing fibers, but their characteristic complex spikes are rarely seen. Changing the stimulation sites within Dc does not appear to change the response pattern but may alter the threshold intensities, latencies and amplitudes. Changing stimulation frequency has complex effects depending on the response type. Purkinje cells responding with initial excitation are located along the lateral edges and along the midline of the corpus cerebelli; units responding with initial inhibition are more often found in an intermediate zone. This suggests three sagittal bands on each side. The contralateral cerebellum has a relative excess of Purkinje cells with initially inhibitory response. Putative eurydendroid cells show either initial excitation or a pattern of inhibition, excitation, inhibition. The initial latency is longer than in Purkinje cells. The contralateral cerebellum has a relative excess of eurydendroid cells with initially excitatory responseThe high proportion of units that respond to Dc stimulation, their complex dynamics, diverse response types and compartmentalization point to the importance of the cerebrocerebellar influence in teleosts. Principal differences from mammals are the much longer latencies and less differentiation according to place stimulation in the cerebrum.

Section: Criteria For Purkinje Cell Spikesmentioning

confidence: 87%

Section: Criteria For Purkinje Cell Spikesmentioning

confidence: 99%

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Cerebellar Units Show Several Types of Early Responses to Telencephalic Stimulation in Catfish

Lee¹,

Bullock²

1990

“…Physiologically, a single action potential in the climbing fiber evokes a large, all-or-none, excitatory postsynaptic potential (EPSP) in the Purkinje cell that in turn evokes postsynaptic spikes. Such climbing fiber responses have been observed in all vertebrates in which Purkinje cells have been recorded, including teleosts [Kotchabhakdi, 1976;V.Z. Han, personal communication], amphibians [Naciemiento, 1969], reptiles [Llinas and Nicholson, 1969], and mammals [Eccles et al, 1967].…”

Section: Cerebellummentioning

confidence: 99%

Evolution of Cerebellum-Like Structures

Bell¹

2002

112

108

All vertebrate brains have a cerebellum, and most of them have one or more additional structures that are histologically similar to the cerebellum. The cerebellum-like structures include the medial octavolateral nucleus in most aquatic vertebrates; the dorsal octavolateral nucleus in many aquatic vertebrates with an electrosensory system; the marginal layer of the optic tectum in ray-finned fishes; electrosensory lobes in the few groups of advanced bony fish with an electrosensory system; the rostrolateral nucleus of the thalamus in a few widely scattered groups of bony fish; and the dorsal cochlear nucleus in all mammals except monotremes. All of these structures receive topographically organized sensory input in their deep layers. Purkinje-like cells receive the sensory input near their cell bodies. These cells extend apical dendrites up into the molecular layer where they receive synaptic input from parallel fibers. The cerebellum itself can be included within this characterization by considering the climbing fiber as at least in part a conveyor of sensory information and by recalling that climbing fibers in more basal vertebrates terminate on smooth dendrites close to the soma. Physiological findings from three different systems suggest the hypothesis that cerebellum-like structures remove predictable features from the sensory inflow. Phylogenetic homology can explain the similarities across different taxa for some types of cerebellum-like structures, but similarities within other types cannot be explained in this way. Moreover, phylogenetic homology cannot explain the similarities among different types of cerebellum-like structures. Evolutionary convergence provides the best explanation for all these similarities that cannot be explained by homology. The convergence is almost surely constrained by the availability of a genetic-developmental program for creating cerebellum-like circuitry and by the need within many different systems for the type of information processing that cerebellum-like circuitry can provide.

“…In mammals, some authors attribute this to simultaneous input from climbing and mossy fibers into the Purkinje cells [Marr, 1969;Albus, 1971;Eccles, 1977;M. Ito, 1982;, If this is true in catfish, the climbing fiber influence is cryptic, since, although they have climbing fibers and the complex spikes they elicit in Purkinje cells [Llinâs and Hillman, 1969;Rawson and Tilokskulchai, 1982], complex spikes are rare in catfish, under the condi tions so far studied, compared to other species, such as goldfish [Kotchabhakdi, 1976].…”

Section: Introductionmentioning

confidence: 99%

Cerebellar Units Show Several Types of Long-Lasting Posttetanic Responses to Telencephalic Stimulation in Catfish

Lee

Bullock²

1990

Extracellular spikes from Purkinje and eurydendroid cells as well as evoked field potentials were recorded from the cerebellum in a catfish following trains of 50–100 stimuli at 2–10 Hz delivered to the area dorsalis centralis (Dc) of the telencephalon. Forty out of 48 Purkinje cells tested showed some response, either an increase or a decrease in the level of ongoing spike discharge following the 10- to 25-second tetanic pulse trains. The altered level lasted for > 3 min. Four out of 16 eurydendroid cells showed an increase in posttrain ongoing discharge; none showed a decrease. In those Purkinje cells responding to single pulse stimulation with early excitation, that response was converted to early inhibition during the later cycles of a tetanic pulse train. When tested with posttrain stimulation, they resumed the pretrain early excitation about 100 s after the train; before that, the recovery stages are complex, neither a simple continuation of, nor a simple rebound from, the later cycles of the stimulus train. Bursting discharge of Purkinje cells is often induced or, if already present, enhanced and regularized, typically at approximately 3/s, by train stimulation of Dc. This pattern begins during the train but continues for tens of seconds after its end. The effects of a stimulus train on the mean frequency and on the pattern of ongoing discharge depend on the train parameters: intensity, duration and stimulus rate within the train; 4–5 Hz is most effective. Higher rates or repeated trains produce a more intense but shorter-lasting effect. Evoked field potentials change during a train, and posttrain test stimuli show a slow recovery, especially after longer pulse trains. The cerebrocerebellar influence in a teleost is nontrivial, widespread, differentiated and shows long-lasting posttetanic plasticity.