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PubMed1994

Sister chromatid separation and the metaphase-anaphase transition in mouse oocytes.

The paper reports on the effect of experimentally inhibiting chromatid separation on meiotic progression and maturation-promoting factor (MPF) activity in both metaphase I (Experiment 1) and metaphase II mouse oocytes (Experiment 2) subjected to combinations of inhibitors of (a) protein synthesis, (b) topoisomerase II, and (c) cytokinesis-cytoskeleton integrity. The results from Experiment 1 showed that the inhibition of protein synthesis invariably results in the extrusion of the first polar body and the formation of an interphase nucleus. Furthermore, this inhibition induces a rapid decline in MPF activity. Similarly, in Experiment 2 the exposure of metaphase II oocytes to cycloheximide initiated a rapid fall in MPF activity, progression to anaphase, the extrusion of the second polar body, and the formation of a pronucleus. While the inhibition of protein synthesis hastened progression through the meiotic cycle, the opposite effect was observed when chromatid separation was prevented by etoposide or colcemid treatment. The results in Experiment 1 demonstrated that the inhibition of chromatid separation totally blocked meiotic progression by preventing the metaphase I to anaphase I transition. These oocytes were characterized by the persistence of high MPF activity for extended periods of time (> 20 hr). This activity declined slowly in oocytes exposed both to inhibitors of chromatin separation and protein synthesis. In Experiment 2 the results showed that the prevention of chromatin separation induced changes which paralleled those observed with MI oocytes. The prevention of chromatid separation with either etoposide or colcemid converted the oocytes from being sensitive to activation stimuli to being entirely resistant to standard activation. In addition, MPF activity remained persistently elevated and declined only when protein synthesis was inhibited. The decline in intracellular MPF activity reached basal levels 6 to 10 hr after the addition of cycloheximide and was accompanied by the slow and gradual decondensation of chromatin. Our results are in accord with those from recent experiments in yeast, insects, and amphibia which suggest that chromatid separation provides an essential signal for cell cycle progression beyond M-phase. We postulate first that exist from both metaphase I and metaphase II, and the characteristic reduction in MPF activity at anaphase in mouse oocytes, are initiated by chromosome (chromatid) separation. Second, we suggest that chemically induced chromosome (chromatid) separation block prevents the anaphase to telophase transition by inhibiting MPF degradation. Third, we postulate that the slow escape from metaphase arrest in oocytes treated with both etoposide and cycloheximide reflects a gradual decrease of MPF activity due to normal protein turnover without new synthesis.

Anaphase↗
PubMed1997

Pattern formation in janus-mutant zebrafish embryos.

Mechanisms that underlie the formation of the vertebrate body appear to be highly conserved between amphibia and teleosts. For teleosts, however, mesoderm induction and the establishment of dorsoventral polarity are poorly understood. In this study, we present an analysis of early pattern formation in the zebrafish maternal-effect mutation janus. This mutation frequently results in a separation of the cleavage stage blastoderm into two halves that undergo separate development until fusion occurs at the end of gastrulation. Here, we employ janus-mutant embryos to analyze the mechanisms of mesoderm formation and ventral specification in a teleost. Analysis of the expression of the panmesodermal marker no tail in janus-mutant embryos indicates that mesoderm induction depends on a marginal position. In an analysis of ventral specification, we show that the early expression of the ventral marker GATA-2 is confined to the area on both blastodermal halves opposite the dorsal shield region. Since, in janus-mutant embryos, the dorsal position is random with respect to the division plane bisecting the two blastodermal halves, a variety of dorsoventral asymmetries arise within individual embryos. In one constellation, the dorsal position is localized to the plane of bisection and two ventral positions develop at opposite ends of the blastodermal halves. Hence, ventral fates can be specified at any position around the blastodermal margins and are excluded from the dorsal position. The diblastodermic system of the janus-mutant embryo allows for the study of the interactions of dorsal and ventral determinants in varying spatial arrangements. We have studied pattern formation in dorsal half-blastoderms that contain the entire shield region but only a reduced ventrolateral marginal zone. As assessed by the presence of the most ventral cell type, blood, ventral specification within a dorsal half-blastoderm is not suppressed.

Animals↗
PubMed2000

Anterior neural induction by nodes from rabbits and mice.

The organizer of vertebrate embryos represents the major regulatory center for the formation of the embryonic axis during gastrulation. The early blastopore lip of amphibia and Hensen's node of the chick at the full-length primitive streak stage possess both a head- and a trunk-inducing potential. In mice, a head-inducing activity was identified in the extraembryonic, anterior visceral endoderm (AVE) by tissue ablation and genetic experiments. Evidence for a similar activity in the AVE from the rabbit was obtained by transplanting below the avian epiblast. However, it was still unclear whether the AVE is the exclusive origin of anterior neural induction or if this activity is recapitulated by the node and/or its derivatives. We report here that nodes from both rabbit and mouse embryos can induce a complete neural axis including forebrain structures upon grafting to chick hosts. Thus, in rabbits and mice not only the AVE, but also the node, possesses a potential for the induction of anterior neural tissue.

Animals↗
PubMed2001

Ecological developmental biology: developmental biology meets the real world.

The production of phenotype is regulated by differential gene expression. However, the regulators of gene expression need not all reside within the embryo. Environmental factors, such as temperature, photoperiod, diet, population density, or the presence of predators, can produce specific phenotypes, presumably by altering gene-expression patterns. The field of ecological developmental biology seeks to look at development in the real world of predators, competitors, and changing seasons. Ecological concerns had played a major role in the formation of experimental embryology, and they are returning as the need for knowledge about the effects of environmental change on embryos and larvae becomes crucial. This essay reviews some of the areas of ecological developmental biology, concentrating on new studies of amphibia and Homo.

Animals↗
PubMed1997

Effects of extracellular matrix components on axonal outgrowth from peripheral nerves of adult animals in vitro.

Relatively little is known of the growth requirements for regenerating axons of the peripheral nervous system of adult animals. In the present study, we show that extracellular matrix material secreted by the Engelbreth-Holm-Swarm tumor cell line (matrigel) supports axonal growth from explanted peripheral nerve-dorsal root ganglia (DRG) preparations of adult mice and amphibia in serum-free media, without addition of growth factors. Axonal growth in matrigel was much more profuse than that in the more commonly used gels of type 1 collagen and, after some days in culture, was accompanied by migration of Schwann cells along axons. The most abundant protein in matrigel is laminin, which has been shown in many studies to support axonal growth but, surprisingly, antisera to laminin did not inhibit axonal growth in matrigel. To determine the ability of the major components of matrigel, laminin, type IV collagen, and heparan sulfate proteoglycan (HSPG), to support axonal growth, these proteins were added to preparations of mouse peripheral nerve-DRGs in type I collagen gels. Regenerating axons were significantly longer in the presence of laminin and type IV collagen than in control cultures, while HSPG had a slight inhibitory effect. In this assay system, however, diluted matrigel solution was even more effective in stimulating axonal growth than laminin or type IV collagen, either alone or in combination. The results suggest that in addition to laminin and type IV collagen, other components within matrigel may contribute to its ability to support axonal growth.

Ambystoma mexicanum↗
PubMed1993

A phylogenetic survey of pancreastatin and chromogranin immunoreactivity in chromaffin (TH-, DBH-, and PNMT-immunoreactive) cells of the adrenal organ of vertebrates.

Region-specific antisera raised against different amino acid sequences of pancreastatin (Pst) (Pst-1-6, Pst-1-17, Pst-14-49 and Pst-33-49) and two antisera towards chromogranin (Cg) A and CgA/B were applied in immunofluorescence to examine the occurrence and distribution of Pst-immunoreactive (-IR) and Cg-IR cells in adrenal organs of several mammals, birds, reptiles, amphibia, and bony fish. The catecholamine-containing cells were identified using antisera against enzymes of catecholamine synthesis (tyrosine-hydroxylase, dopamine-beta-hydroxylase, and phenylethanolamine-N-methyl-transferase). No animal showed any Pst-IR or Cg-IR cells in the adrenal cortex or in its homolog, the interrenal. All antisera reacted with chromaffin cells in porcine adrenal medulla. Both adrenaline (A)- and noradrenaline (NA)-containing cells displayed Pst- and Cg-immunoreactivity. Pst- and CgA-immunoreactivities were observed in coexistence using double immunofluorescence. However, strongly reacting Pst-IR cells showed only low CgA immunoreactivity and vice versa. This inverse relationship between Pst- and CgA-immunoreactivities might reflect different levels of processing of the likely Pst-precursor CgA. In all nonmammalian vertebrates studied, Pst- and Cg-immunoreactivities were also found in both A- and NA-containing adrenal cells. However, the chromaffin cells reacted only with the antisera Pst-1-6, Pst-1-17, Pst-33-49, and CgAB. The adrenal chromaffin cells of nonmammalian vertebrates appear to contain Pst-/Cg-like peptides akin to those of the enteroendocrine cells but different from those of their endocrine pancreas. Since no immunoreactions were obtained with antiserum CgA, nonmammalian Pst may be derived from a precursor different from mammalian CgA.

Adrenal Glands↗
PubMed1996

Isolation and structural characterization of proglucagon-derived peptides, pancreatic polypeptide, and somatostatin from the urodele Amphiuma tridactylum.

The expression of the preproglucagon gene in vertebrates is markedly species- and tissue-dependent. Three peptides derived from the posttranslational processing of preproglucagon were isolated from an extract of the pancreas of the urodele Amphiuma tridactylum (threetoed amphiuma). The primary structures of the peptides indicated identity with glucagon (HSQGTFTSDY10 SKYLDNRRAQ20 DFIQWLMST), glucagon-like peptide-1 (GLP-1) (HADGTLTSDI10 SSFLEKQATK20 EFIAWLVSGR30 GRRQ), and glucagon-like peptide-2 (GLP-2) (HADGSFTSDI10 NKVLDTIAAK20 EFLNWLISTK30 VTE). Thus, in a urodele, as in the bullfrog but in contrast to the chicken and all nontetrapod species yet studied, pancreatic preproglucagon mRNA encodes a GLP-2 sequence. The amino acid sequence of glucagon has been better conserved during evolution of tetrapods (3 substitutions between amphiuma and human) than the sequences of either GLP-1 (7 substitutions) or GLP-2 (15 substitutions). Pancreatic polypeptide was also isolated from the extract and its primary structure (APKEPEHPGD10 DASPEQLEKY20 YQDLFQYIIF30 ITRPRY.NH2) indicates that the amino acid sequence of this peptide has been very poorly conserved, even among the amphibia. Amphiuma pancreatic somatostatin is identical to mammalian somatostatin-14.

Amino Acid Sequence↗
PubMed1996

3,5,3'-Triiodo-L-thyronine and L-thyroxine uptake into red blood cells of rainbow trout, Oncorhynchus mykiss.

Uptake of the thyroid hormones (TH) 3,5,3'-triiodo-L-thyronine (T3) and L-thyroxine (T4) by trout red blood cells (RBC) was studied by incubating washed RBC in a balanced salts medium containing glucose and [125I]TH at the fish acclimation temperature of 12 degrees. RBC were separated from the medium by centrifugation through silicone oil and glycine buffer (pH 10.5). Maximal [125I]T3 uptake occurred by 10-15 min, but not by 60 min for [125I]T4. First-order uptake was measured at 30 sec for T3 and at 90 sec for T4. Total T4 uptake was enhanced 15-fold from pH 8 to 6 and was affected most below pH 7.2; total T3 uptake was maximal between pH 6.4 and 7.0, but was relatively insensitive to pH. At 0.2 nM, nonsaturable uptake of T3 exceeded that of T4 3- to 6-fold, accounting for 3% (T3) and 50% (T4) of total uptake. Saturable TH uptake was described by Michaelis-Menten kinetics. The saturable transport system for T3 had an apparent K(t) (carrier affinity) of 70-119 nM and J(max) (maximal uptake velocity) of 540-1116 pmol . 10(6) cells(-1) . min(-1). A saturable system was also found for T4, with an apparent K(t) of 99 pM-1.1 nM and J(max) of 8-77 fmol . 10(6) cells(-1) . min(-1). Saturable uptake of both TH depended on temperature. Activation energies for the nonsaturable component were 48 (T4) and 64 (T3) KJ . mol(-1) over the range 0-21 degrees. Activation energies for the saturable components were 52 KJ . mol(-1) (T4, 0-21 degrees), 52 KJ . mol(-1) (T3, 0-10 degrees), and 3 KJ . mol(-1) (T3, 10-21 degrees). During a 16-month study saturable and nonsaturable uptake of both TH increased, probably due to fish age. We conclude that in trout RBC, rapid T3 uptake by a pH- and temperature-sensitive saturable carrier greatly exceeds T4 uptake. The rate of T3 uptake exceeds by 100- to 1000-fold that of mammals and amphibia, and in contrast to those taxa some saturable T4 uptake also occurs.

Aging↗
PubMed1996

Plasma thyroxine concentrations in farmed ostriches in relation to age, body weight, and growth hormone.

Thyroid hormones are of interest in ostriches because, in common with other ratites, ostriches are believed to have evolved through neoteny, a process which, in amphibia, is related to thyroid function. Farmed ostriches show marked differences in growth rates, a problem which also could be related to abnormal thyroid function. In adult farmed ostriches (more than 3 years old), mean plasma thyroxine concentration was 1.8 nmol middle dot liter-1 (range 0.2 to 6.5 nmol middle dot liter-1). This is a lower mean and a much greater range than those in adult starlings or Japanese quail measured at the same time. No sex differences were observed. In 5-month-old ostriches (approximately half grown) mean levels were again low (3.1 nmol x liter-1, range 0.2 to 9.9 nmol x liter-1). There was a correlation (P < 0.0005) between thyroxine and body weight, which ranged from 10.8 to 51.5 kg. Growth hormone in this group ranged from 0.7 to 45.6 microg x liter-1, but there was no correlation with body weight or with thyroxine. In the same group of birds at 10 months of age, plasma thyroxine concentrations were similar, but were not correlated with body weight. In young birds sampled between hatch and 13 weeks, mean thyroxine decreased from 7.6 nmol x liter-1 soon after hatching to less than 2 nmol x liter-1 at 2 weeks and remained less than 2 nmol x liter-1 for the following 3 months. Thyroxine was highly variable within and between individuals. There was no correlation with body weight or growth rate. There were no significant differences between values at 13 weeks, 5 months, 10 months, or in adults. The results do not suggest that slow growth is directly related to low thyroxine. However, the low means and wide range of values do suggest that thyroid function in the ostrich is abnormal compared to other birds.

Aging↗
PubMed1999

Evolution and physiology of the corticotropin-releasing factor (CRF) family of neuropeptides in vertebrates.

Corticotropin-releasing factor (CRF), urotensin-I, urocortin and sauvagine belong to a family of related neuropeptides found throughout chordate taxa and likely stem from an ancestral peptide precursor early in metazoan ancestry. In vertebrates, current evidence suggests that CRF on one hand, and urotensin-I, urocortin and sauvagine, on the other, form paralogous lineages. Urocortin and sauvagine appear to represent tetrapod orthologues of fish urotensin-I. Sauvagine's unique structure may reflect the distinctly derived evolutionary history of the anura and the amphibia in general. The physiological actions of these peptides are mediated by at least two receptor subtypes and a soluble binding protein. Although the earliest functions of these peptides may have been associated with osmoregulation and diuresis, a constellation of physiological effects associated with stress and anxiety, vasoregulation, thermoregulation, growth and metabolism, metamorphosis and reproduction have been identified in various vertebrate species. The elaboration of neural circuitry for each of the two paralogous neuropeptide systems appears to have followed distinct pathways in the actinopterygian and sarcopterygian lineages of vertebrates. A comparision of the functional differences between these two lineages predicts additional functions of these peptides.

Amino Acid Sequence↗
PubMed1996

Discovery of amphibian Tc1-like transposon families.

We have discovered transposase sequences in the bull frog (Rana catesbeiana) and in the clawed frog (Xenopus laevis), which demonstrates that there are DNA-mediated transposons in Amphibia. The DNA sequences of 11 new Xenopus elements describe two new vertebrate transposon families. Phylogenetic analysis, using these sequences along with previously defined vertebrate and invertebrate elements, reveals at least five families of Tc1-like elements in Vertebrata. Some of these families co-exist in the same genome. Furthermore, the grouping of one of the amphibian transposon families with a branch of the teleost transposons raises the possibility of horizontal transfer.

Amino Acid Sequence↗
PubMed2000

Immunohistochemical demonstration of hyaluronan and its possible involvement in axolotl neural crest cell migration.

Hyaluronan (HA), an extracellular matrix component, is involved mainly in the control of cell proliferation, neural crest and tumor cell migration, and wound repair. We investigated the effect of hyaluronan on neural crest (NC) cell migration and its ultrastructural localization in dark (wild-type) and white mutant embryos of the Mexican axolotl (Ambystoma mexicanum, Amphibia). The axolotl system is an accepted model for studying mechanisms of NC cell migration. Using a biotinylated hyaluronan binding protein (HABP), major extracellular matrix (ECM) spaces, including those of NC cell migration, reacted equally positive on cryosections through dark and white embryos. Since neural crest-derived pigment cells migrate only in subepidermal spaces of dark embryos, HA does not seem to influence crest cell migration in vivo. However, when tested on different alternating substrates in vitro, migrating NC cells in dark and white embryos prefer HA to fibronectin. In vivo, such an HA migration stimulating effect might exist as well, but be counteracted to differing degrees in dark and white embryos. The ultrastructural localization of HA was studied by means of transmission electron microscopic immunohistochemistry using HABP and different protocols of standard chemical fixation, cryofixation, embedding, and immunolabeling. The binding reaction of HA to HABP was strong and showed an equal distribution throughout ECM spaces after both standard chemical fixation/freeze substitution and cryofixation. A preference for the somite or subepidermal side was not observed. Following standard fixation/freeze substitution HABP-labeled "honeycomb"-like networks reminiscent of fixation artifacts were more prominent than labeled fibrillar or irregular net-like structures. The latter predominated in adequately frozen specimens following high-pressure freezing/freeze substitution. For this reason fibrillar or irregular net-like structures very likely represent hyaluronan in the complex subepidermal matrix of the axolotl embryo in its native arrangement.

Ambystoma↗
PubMed2000

Why and how marine-invertebrate larvae metamorphose so fast.

It is argued that larviparous development has evolved at least eight times among extant animals. A 'need for speed hypothesis' is proposed to explain profound convergence on a pattern of small larvae and rapid metamorphosis across six marine invertebrate clades. Shared selection pressures include limits to larval size, the plankton-to-benthos transition, extreme hazards on the benthos, and the profound helplessness of metamorphosing animals. The adaptive mechanisms include: (1) development of juvenile structures in larvae before they are metamorphically competent; (2) external cues trigger metamorphosis; and (3) rapid cell-to-cell conductance of the metamorphic signal to bring about rapid loss of larval structures and release of juvenile structures. Both pattern and mechanisms contrast in every regard with those of the other two major larviparous clades, Insecta and Amphibia.

Adaptation, Physiological↗
PubMed1975

Phylogeny of functional humoral transplantation immunity: comparative studies in amphibians and rodents.

Remarkably comparable observations from parallel experiments in salamanders and mice utilizing three related model systems (implant-induced immunomanipulation; passive transfer; and putative B cell suppression) argue directly that functional humoral transplantation immunity is highly developed at the phylogenetic level of Amphibia and that it plays a major role in regulating graft survival in these species (Fig. 4). Although it is still conjectural whether such humoral immunity and weak H-antigens evolved concurrently, the argument that enhancing atibodies evolved exclusively in viviparous species to protect the fetus from potential rejection by the maternal immune system no longer seems tenable (1).

Animals↗
PubMed1993

The efferent system of cranial nerve nuclei: a comparative neuromorphological study.

A number of inconsistencies and controversies are inherent in the classification of cranial nerve nuclei based on the concepts of the various head-theories. The assumption of head segmentation, which is common to these theories, serves as the basis for designating the dorsomedial nuclei as the somatomotor column, although they innervate striated muscles of a viscus and a specific sense organ. The ventrolateral nuclei are called the specific visceromotor column; they innervate striated muscles in the branchiogenous area, but many of these muscles insert on skeletal elements. A series of comparative neuromorphological studies investigating the dendritic arborization pattern and axonal trajectory in the frog, lizard, and rat suggests a much more delicate classification in which nine morphologically and functionally different neuron groups can be discerned: 1. The hypoglossal nucleus appears coincidentally with the muscular tongue in amphibia. The spindle-shaped perikaryon, the bipolar dendritic arborization, and the straight ventral trajectory of the axon are characteristic morphological features in all three animal species investigated. 2. The oculomotor, trochlear, and abducens nuclei present a remarkably conservative topography and organization in all vertebrates with a moving eye. With their oval-shaped or polygonal perikarya and radiating dendritic arborization, these neurons distinctly differ from hypoglossal neurons. The ipsilateral axons follow a straight ventral course, the contralateral axons form a dorsal loop before crossing the midline, and the crossing is not consequence of neuron migration to the contralateral side. 3. The accessory abducens nucleus is present in tetrapods except apes and human. The elongated perikaryon and the dorsoventral dendritic orientation distinctly distinguish these neurons from other cranial motoneurons, the nucleus is found in the lateral part of the reticular formation. The neurons differentiate in situ, they do not migrate from the main abducens nucleus. 4. In the submammalian trigeminal and facial nuclei, two basic neuron types can be distinguished on the basis of their morphology. The first type is larger and accumulates in the rostral part of the trigeminal nucleus. This type innervates the jaw closer muscles. The second type is found in the caudal part of the trigeminal nucleus and in the facial nucleus. These neurons innervate the muscular floor of the mouth and the facial contingent supplies the jaw opener muscle. A very characteristic feature in the axonal trajectory is an initial medial course and a hairpin turn, or dorsal loop, at the lateral aspect of the medial longitudinal fasciculus. In addition to the two types of neurons, there is a third type in the frog trigeminal nucleus. This innervates an orbital muscle.(ABSTRACT TRUNCATED AT 400 WORDS)

Abducens Nerve↗
PubMedDate not supplied

Further evidence for early sex chromosome differentiation of anuran species.

Chromosome banding and meiotic evidence show that XX/XY systems found in two Eupsophus species (Amphibia-Leptodactylidae) represent early stages of sex chromosome differentiation. Pair 14 is heteromorphic in E. migueli males and represents the heterochromosomes. In E. roseus this pair is metacentric and does not show heteromorphism. Paracentromeric constitutive heterochromatin is present in all chromosomes except in the E. migueli and E. roseus metacentric Y chromosomes. Constitutive heterochromatin loss is the structural modification responsible for Y chromosome differentiation. Pericentric inversions may have modified the morphology of the X chromosome of Eupsophus species.

Animals↗
PubMed1994

Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene.

The phylogenetic relationships among Primates (human), Artiodactyla (cow), Cetacea (whale), Carnivora (seal), and Rodentia (mouse and rat) were estimated from the inferred amino acid sequences of the mitochondrial genomes using Marsupialia (opossum), Aves (chicken), and Amphibia (Xenopus) as an outgroup. The overall evidence of the maximum likelihood analysis suggests that Rodentia is an outgroup to the other four eutherian orders and that Cetacea and Artiodactyla form a clade with Carnivora as a sister taxon irrespective of the assumed model for amino acid substitutions. Although there remains an uncertainty concerning the relation among Artiodactyla, Cetacea, and Carnivora, the existence of a clade formed by these three orders and the outgroup status of Rodentia to the other eutherian orders seems to be firmly established. However, analyses of individual genes do not necessarily conform to this conclusion, and some of the genes reject the putatively correct tree with nearly 5% significance. Although this discrepancy can be due to convergent or parallel evolution in the specific genes, it was pointed out that, even without a particular reason, such a discrepancy can occur in 5% of the cases if the branching among the orders in question occurred within a short period. Due to uncertainty about the assumed model underlying the phylogenetic inference, this can occur even more frequently. This demonstrates the importance of analyzing enough sequences to avoid the danger of concluding an erroneous tree.

Animals↗
PubMed1975

The general ultrastructure of the carotid body of the domestic fowl.

Electron microscopic studies of the carotid body of the domestic fowl (Gallus gallus domesticus) have shown Type I and Type II cells combined with axons into compact groups. The many Type I cells in the depths of the organ had a body, containing the nucleus, and an elongated, flared process. Some of the Type I cells in the superficial regions tended to be spindle-shaped. Type I cells were characterised by membrane-bound, dense-cored vesicles about 120 nm in diameter. Type II cells invested the Type I cells and had axons embedded in them as in Schwann cells. The fine structure of the carotid body in the domestic fowl resembles that of the Lovebird (Uroloncha domestica) and of various amphibia and mammals. The possibility is discussed that the Type I cells may have a chemoreceptor or a general secretory function, or even both of these axons leading to or from Type I cells. The main role of the Type II cells seems to be to provide a pathway for functions together.

Animals↗