Cytoarchitecture of the telencephalon in the coral reef multiband Butterflyfish ( Chaetodon multicinctus : Perciformes).

Detailed neuroanatomical studies of model species are necessary to facilitate comparative experiments which test hypotheses relevant to brain evolution and function. Butterflyfishes (Chaetodontidae) boast numerous sympatric species that differ in social behavior, aggression and feeding ecology. However, the ability to test hypotheses relevant to brain function in this family is hindered by the lack of detailed neural descriptions. The cytoarchitecture of the telencephalon in the monogamous and territorial multiband butterflyfish, Chaetodon multicinctus, was determined with Nissl-stained serial sections and an immunohistochemical analysis of arginine vasotocin (AVT), serotonin, substance P and tyrosine hydroxylase. The ventral telencephalon was similar to that of other perciform fishes studied, with one major difference. A previously undescribed postcommissural region, the cuneate nucleus, was identified and putatively assigned to the ventral telencephalon. While the function of this nucleus is unknown, preliminary studies indicate that it may be part of a behaviorally relevant subpallial neural circuit that is modulated by AVT. The dorsal telencephalon consisted of 15 subdivisions among central, medial, lateral, dorsal and posterior zones. Several regions of the dorsal telencephalon of C. multicinctus differed from many other perciform fishes examined thus far. The nucleus taenia was in a more caudal position, and the central and lateral zones were enlarged. Within the lateral zone, an unusual third, ventral subdivision and a large-celled division were present. One hypothesis is that the enlarged ventral subdivision of the lateral zone (potential hippocampus homolog) relates to an enhancement of spatial learning or olfactory memory, which are important for this coral reef fish. This study provides the neuroanatomical basis for future comparative and evolutionary studies of brain organization and neuropeptide distributions, physiological studies of neural processing and insight into the complex social behavior of butterflyfishes.

Fast drum strokes: novel and convergent features of sonic muscle ultrastructure, innervation, and motor neuron organization in the Pyramid Butterflyfish (Hemitaurichthys polylepis).

Sound production that is mediated by intrinsic or extrinsic swim bladder musculature has evolved multiple times in teleost fishes. Sonic muscles must contract rapidly and synchronously to compress the gas-filled bladder with sufficient velocity to produce sound. Muscle modifications that may promote rapid contraction include small fiber diameter, elaborate sarcoplasmic reticulum (SR), triads at the A-I boundary, and cores of sarcoplasm. The diversity of innervation patterns indicate that sonic muscles have independently evolved from different trunk muscle precursors. The analysis of sonic motor pathways in distantly related fishes is required to determine the relationships between sonic muscle evolution and function in acoustic signaling. We examined the ultrastructure of sonic and adjacent hypaxial muscle fibers and the distribution of sonic motor neurons in the coral reef Pyramid Butterflyfish (Chaetodontidae: Hemitaurichthys polylepis) that produces sound by contraction of extrinsic sonic muscles near the anterior swim bladder. Relative to adjacent hypaxial fibers, sonic muscle fibers were sparsely arranged among the endomysium, smaller in cross-section, had longer sarcomeres, a more elaborate SR, wider t-tubules, and more radially arranged myofibrils. Both sonic and non-sonic muscle fibers possessed triads at the Z-line, lacked sarcoplasmic cores, and had mitochondria among the myofibrils and concentrated within the peripheral sarcoplasm. Sonic muscles of this derived eutelost possess features convergent with other distant vocal taxa (other euteleosts and non-euteleosts): small fiber diameter, a well-developed SR, and radial myofibrils. In contrast with some sonic fishes, however, Pyramid Butterflyfish sonic muscles lack sarcoplasmic cores and A-I triads. Retrograde nerve label experiments show that sonic muscle is innervated by central and ventrolateral motor neurons associated with spinal nerves 1-3. This restricted distribution of sonic motor neurons in the spinal cord differs from many euteleosts and likely reflects the embryological origin of sonic muscles from hypaxial trunk precursors rather than occipital somites.

Arginine vasotocin neuronal phenotypes and their relationship to aggressive behavior in the territorial monogamous multiband butterflyfish, Chaetodon multicinctus.

Intra and interspecific comparisons of arginine vasotocin (AVT) and its mammalian homolog arginine vasopressin (AVP) demonstrate several relationships between these neuropeptides and aggression/dominance behaviors. Prior studies in coral reef butterflyfishes and other fishes indicate that features of AVT neurons in the gigantocellular preoptic area (gPOA) and axon varicosities within the ventral nucleus of the ventral telencephalon should have a positive relationship with aggressive behavior, whereas AVT-ir neuronal features in the parvocellular preoptic area (pPOA) should have a negative relationship. We measured the offensive aggression of wild caught territorial monogamous multiband butterflyfish, Chaetodon multicinctus, in a simple lab paradigm that controlled for social context and variations in social stimuli. Offensive aggression did not follow a clear stereotyped pattern, but rather a complex sequence that includes five action patterns and two approach behaviors. We then used immunohistochemistry to test for associations between AVT immunoreactive features and projections with overall offensive aggression. Our results indicate that gPOA cell number was positively related to aggression while both the size and number of pPOA cells were negatively related to aggression. No association between aggression and the number of axon varicosities in the telencephalic region proposed to be associated with aggression was found. This study provides further support for the relationship between AVT neuronal features and aggression in fishes, and provides preliminary evidence that this relationship may relate to the motivation to produce aggressive behaviors in the immediate future.

Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals.

The neuropeptide arginine vasopressin (AVP) influences many social behaviors through its action in the forebrain of mammals. However, the function of the homologous arginine vasotocin (AVT) in the forebrain of fishes, specifically the telencephalon remains unresolved. We tested whether the density of AVT-immunoreactive (-ir) fiber varicosities, somata size or number of AVT-ir neuronal phenotypes within the forebrain were predictive of social behavior in reproductive males of seven species of butterflyfishes (family Chaetodontidae) in four phylogenetic clades. Similar to other fishes, the aggressive (often territorial) species in most cases had larger AVT-ir cells within the gigantocellular preoptic cell group. Linear discriminant function analyses demonstrated that the density of AVT-ir varicosities within homologous telencephalic nuclei to those important for social behavior in mammals and birds were predictive of aggressive behavior, social affiliations, and mating system. Of note, the density of AVT-ir varicosities within the ventral nucleus of the ventral telencephalon, thought to be homologous to the septum of other vertebrates, was the strongest predictor of aggressive behavior, social affiliation, and mating system. These results are consistent with the postulate that AVT within the telencephalon of fishes plays an important role in social behavior and may function in a similar manner to that of AVT/AVP in birds and mammals despite having cell populations solely within the preoptic area.