Decussation Geometries in the Goldfish Nervous System

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Decussation Geometries in the Goldfish Nervous System Proc. Natl. Acad. Sci. USA Vol. 76, No. 8, pp. 4131-4135, August 1979 Neurobiology Decussation geometries in the goldfish nervous system: Correlation with probability of survival (brain asymmetries/lateralization of function/Mauthner's neuron/optic chiasm/natural selection) RICHARD L. ROTH Department of Biological Sciences, Stanford University, Stanford, California 94305 Communicated by Donald Kennedy, May 9, 1979 ABSTRACT In the goldfish, the optic nerve decussation assumed to be representative of goldfish available in the United occurs without intermingling of fibers from the two eyes. In States. The embryonic and larval specimens examined were two-thirds of juvenile and adult specimens, the left optic nerve derived from two lots of fertile eggs and, by the breeders' es- is dorsal at the midline. In about 60% of the specimens, the decussation of Mauthner's neuron also has a left-dorsal-to-right timates, represent the progeny of 9-14 spawning females.* (L/R) configuration. Concordance for decussation geometry is Despite this limited sampling of embryos and larvae, the results greater than 80%, with smaller specimens accounting for a presented below indicate that they, too, provide an adequate disproportionate number of discordant cases. In embryos and basis for generalization. very young larvae, the L/R configuration occurs in slightly less For minimization of sampling bias, most of the Spanish moss than 50% of o tic chiasmata and in slightly more than 50% of into each Mauthner's cell chiasmata, and there is no significant tendency containing the eggs was teased and cut portions, toward concordance. However, larval specimens that survive bearing 50-75 eggs. These portions were distributed sequen- 1 month after hatching are markedly skewed toward adult de- tially among 10 aquaria so that each aquarium contained every cussation patterns and somewhat skewed toward concordance. tenth sample of eggs. From the remainder of the Spanish moss, These observations, together with results of cannibalization and individual eggs were isolated, and these singlets were distrib- predation experiments, suggest that the adult population pattern uted among trios of 1-gallon aquaria so that, as defined by the can be achieved through selection pressures against discordant individuals and, perhaps separately, against individuals with order of selection, one aquarium contained specimens 1, 4 ..., right-dorsal-to-left (R/L) chiasmatic configurations. Decussation n -2; a second contained specimens 2, 5, .. -,n-1; and a third patterns correlate with embryonic postures, larval orientation contained specimens 3, 6, . n. Some of these randomized preferences, and growth rates after hatching, which may samples were killed in their entirety at 1 day to 1 week after themselves serve as a basis for selection. hatching and used to establish a larval population base line with respect to optic and M-cell chiasmatic geometries. Others were Recent studies of lateral asymmetries in nervous systems have subsampled in a variety of ways, which are detailed below. been directed not only toward further cataloging of functional Maintenance of Embryos and Larvae. Eggs were main- asymmetries, but also toward examining the morphological tained in water treated with methylene blue, Fungizone, or a (1-5) and biochemical (6) asymmetries that may underlie la- Fungizone/penicillin mixture (GIBCO) to retard fungal and teralization of function. Among the efforts to define anatomical fed either asymmetries have been attempts to correlate geometric con- bacterial infections. Free-swimming larvae were figuration of the pyramidal tract decussation with "handedness" infusoria or sieved hard-boiled egg yolk, and water was changed (2) and to define a genetic basis for different decussation as necessary. geometries of the optic nerves and Mauthner cell (M-cell) axons Histological Procedures and Determination of Chiasmatic in teleost fish (7). These studies of asymmetry in decussation Configurations. Virtually all the juvenile and adult specimens patterning have produced equivocal results because functional on which this report is based had initially been used in other correlations could not be tested (5) 6r because of small or po- investigations in which it became an incidental practice to tentially biased samples (2, 7). record the configurations of optic chiasmata as brains were The present investigation of asymmetries in decussation being removed for histological processing. This earlier work geometries exhibited by the M-cells and optic nerves of the yielded a large library of Bodian-stained serial sections. Al- goldfish overcomes some of these problems by use of large though the M-cell was not included in sections of most of these samples, by following randomized samples from embryonic specimens and the optic chiasm was not included in others, the through late larval stages, and by sorting previously randomized configuration of the M-cell chiasm could be determined in more to a of and behavioral than 100 individuals and that of both optic and M-cell chi- samples according variety postural asmata in more than 80. The sample used to determine optic asymmetries. chiasmatic pattern included, in addition to specimens in this MATERIALS AND METHODS slide collection, approximately 100 poorly fixed specimens in which the optic chiasm was scored only by dissection. Structure of Samples. This report is based on the examina- Preparation of all larval specimens was according to the tion of more than 250 juvenile or adult and more than 1000 standard Bodian method. To facilitate accuracy in scoring of embryonic or larval goldfish (Carassius auratus). Because the juvenile and adult specimens were obtained over the past 14 Abbreviations: M-cell, Mauthner's neuron; L/R, left-dorsal-to-right; years from several distributors in Ohio and California, they are R/L, right-dorsal-to-left. * One lot of eggs, representing "domestic" stock and provided by Ozark The publication costs of this article were defrayed in part by page Fisheries, Inc. (Stoutland, MO), was produced by 8-12 females. The charge payment. This article must therefore be hereby marked "ad- other, representing recently imported Japanese stock and provided vertisement" in accordance with 18 U. S. C. §1734 solely to indicate by Golden State Hatcheries, Inc. (Winters, CA), was produced by this fact. one or two females. 4131 Downloaded by guest on September 27, 2021 4132 Neurobiology: Roth Proc. Natl. Acad. Sci. USA 76 (1979) decussation patterns, conventions were uniform with respect Table 2. Preponderance of concordant chiasmatic configurations to orientation of specimens in the paraffin blocks, orientation in a sample of 81 juvenile and adult goldfish of paraffin ribbons on slides, and orientation of finished slides M-cell chiasm on the microscope stage. Each specimen was scored first with Optic L/R R/L respect to its apparent orientation in the microscopic field, then chiasm Obs. Exp. Obs. Exp. Total with respect to the apparent relationship between chiasmatic L/R n 42 29 8 21 components. Only after a permanent record of these apparent 50 f 0.518 0.358 0.099 0.259 0.617 relationships had been made were apparent relationships converted to the actual ones by defining the axes of the indi- R/L n 5 18 26 13 31 vidual specimen. f 0.062 0.222 0.321 0.161 0.383 RESULTS Total n 47 34 81 f 0.580 0.420 The optic and M-cell chiasmatic configurations in the sample Heavy lines indicate division of the sample into the four compart- of juvenile and adult specimens are summarized in Table 1. ments jointly defined by the geometries of the optic and M-cell chi- Because this sample was drawn about equally from midwestern asmata. Concordant cases appear in the upper left and lower right and west coast suppliers and because the frequencies of the two compartments. Each compartment shows the number of cases ex- chiasmatic geometries were nearly identical for the two sub- pected if chiasmatic patterns are independent and the number ob- samples, the data were pooled. The critical points are (i) the served. n, Number; f, frequency; Obs., observed; Exp., expected. population frequency of left-dorsal-to-right Differences between observed and expected values are highly sig- (L/R) configura- nificant (X2 = 36.19, P << 0.001). tions must be very nearly 0.67 for the optic chiasm and 0.59 for the M-cell chiasm, and (ii) the differences in frequency of L/R configurations of the two chiasmata are significant. Restructuring of larval populations is evident within a few Considered separately, these asymmetries in pattern might weeks of hatching. Table 4 summarizes the distribution of be interpreted as trivial accidents of development. However, chiasmatic configurations in 3- to-6-week-old survivors of ini- those specimens in which both chiasmata could be examined tially randomized samples (matched to those killed at 1-7 days suggested that patterning of decussations might be of consid- after hatching). In this older population the asymmetric dis- erable importance. As shown in Table 2, the configurations of tribution of chiasmatic geometries approaches that of the ju- optic and M-cell chiasmata are neither independent of each venile/adult sample. This population restructuring is evidently other (in which case concordance for pattern would be about the result of selective cannibalization among larvae of the same 50%) nor are they rigorously predisposed to a common pattern chronological age rather than of differential low resistance to (in which case concordance would be perfect). One might still infection or of postembryonic expression of lethal genes or se- argue that the imperfect (80%) concordance results from partial rious developmental anomalies. Those recently dead or mori- dependence on some common event or condition during em- bund specimens in which decussation patterns could be de- bryogenesis were it not for the observation that discordant termined represented all four population compartments in the patterns were more common in the smaller members of this proportions expected on the basis of chronological age.
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