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Cytoarchitecture of the Telencephalon in the Coral Reef Multiband Butterflyfish (Chaetodon Multicinctus: Perciformes)

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Original Paper Brain Behav Evol 2014;84:31–50 Received: June 24, 2013 DOI: 10.1159/000363124 Returned for revision: August 12, 2013 Accepted after second revision: April 22, 2014 Published online: August 14, 2014 Cytoarchitecture of the Telencephalon in the Coral Reef Multiband Butterflyfish (Chaetodon multicinctus : Perciformes) a, b a, b Adam K. Dewan Timothy C. Tricas a b Department of Biology, and Hawai’i Institute of Marine Biology, University of Hawai’i at Manoa, Honolulu, Hawaii , USA Key Words divisions among central, medial, lateral, dorsal and posterior Neuroanatomy · Forebrain · Teleost · zones. Several regions of the dorsal telencephalon of C. mul- Immunohistochemistry · Behavior · Chaetodontidae ticinctus differed from many other perciform fishes exam- ined thus far. The nucleus taenia was in a more caudal posi- tion, and the central and lateral zones were enlarged. Within Abstract the lateral zone, an unusual third, ventral subdivision and a Detailed neuroanatomical studies of model species are nec- large-celled division were present. One hypothesis is that essary to facilitate comparative experiments which test hy- the enlarged ventral subdivision of the lateral zone (poten- potheses relevant to brain evolution and function. Butterfly- tial hippocampus homolog) relates to an enhancement of fishes (Chaetodontidae) boast numerous sympatric species spatial learning or olfactory memory, which are important that differ in social behavior, aggression and feeding ecolo- for this coral reef fish. This study provides the neuroanatom- gy. However, the ability to test hypotheses relevant to brain ical basis for future comparative and evolutionary studies of function in this family is hindered by the lack of detailed neu- brain organization and neuropeptide distributions, physio- ral descriptions. The cytoarchitecture of the telencephalon logical studies of neural processing and insight into the com- in the monogamous and territorial multiband butterflyfish, plex social behavior of butterflyfishes. Chaetodon multicinctus, was determined with Nissl-stained © 2014 S. Karger AG, Basel serial sections and an immunohistochemical analysis of argi- nine vasotocin (AVT), serotonin, substance P and tyrosine hy- droxylase. The ventral telencephalon was similar to that of Introduction other perciform fishes studied, with one major difference. A previously undescribed postcommissural region, the cune- Our understanding of the neural regulation of behav- ate nucleus, was identified and putatively assigned to the ior is dependent upon detailed neuroanatomical and con- ventral telencephalon. While the function of this nucleus is nectome studies. When these studies are compared across unknown, preliminary studies indicate that it may be part of non-model species (which display differences in behavior a behaviorally relevant subpallial neural circuit that is modu- or ecological niche), variations in their neuroanatomy lated by AVT. The dorsal telencephalon consisted of 15 sub- can highlight behaviorally relevant circuits. For example, © 2014 S. Karger AG, Basel Adam K. Dewan 0006–8977/14/0841–0031$39.50/0 Department of Neurobiology, Northwestern University 2205 Tech Drive, Hogan 2-160 E-Mail [email protected] Evanston, IL 60208 (USA) www.karger.com/bbe E-Mail a-dewan @ northwestern.edu Downloaded by: University of Hawaii Library 128.171.57.189 - 9/12/2014 7:50:07 PM Abbreviations used in this paper 5-HT serotonin HYP hypothalamus A C anterior commissure ICL internal cell layer of the olfactory bulb AVT arginine vasotocin I I optic tract C caudal i r immunoreactive CER cerebellum LFB lateral forebrain bundle D dorsal L T left D c central zone of the dorsal telencephalon NGS normal goat serum Dc1 central zone of the dorsal telencephalon, division 1 N T nucleus taenia Dc2 central zone of the dorsal telencephalon, division 2 O B olfactory bulb D d dorsal zone of the dorsal telencephalon o c optic chiasm D l lateral zone of the dorsal telencephalon OLN olfactory nerve fiber layer of the olfactory bulb Dld dorsal division of the lateral zone of the dorsal POA preoptic area telencephalon PSp parvocellular superficial pretectal nucleus Dlp posterior division of the lateral zone of the dorsal R T right telencephalon S unknown sulcus Dlv ventral division of the lateral zone of the dorsal S e sulcus externus telencephalon S l sulcus limitans Dlv1 ventral division of the lateral zone of the dorsal Slat sulcus lateralis telencephalon, subdivision 1 SOF secondary olfactory layer of the olfactory bulb Dlv2 ventral division of the lateral zone of the dorsal S P substance P telencephalon, subdivision 2 S y sulcus ypsiloniformis Dlv3 ventral division of the lateral zone of the dorsal T optic tectum telencephalon, subdivision 3 T C tela choroidea D m medial zone of the dorsal telencephalon TEL telencephalon Dm1 medial zone of the dorsal telencephalon, division 1 T H tyrosine hydroxylase Dm2 medial zone of the dorsal telencephalon, division 2 V ventral Dm3 medial zone of the dorsal telencephalon, division 3 V c central nucleus of the ventral telencephalon Dm4 medial zone of the dorsal telencephalon, division 4 V d dorsal nucleus of the ventral telencephalon D p posterior zone of the dorsal telencephalon V i intermediate nucleus of the ventral telencephalon large-cell division of the lateral zone of the dorsal V l lateral nucleus of the ventral telencephalon D x telencephalon V p postcommissural nucleus of the ventral telencephalon E entopeduncular nucleus of the ventral telencephalon V s supracommissural nucleus of the ventral telencephalon ECL external cell layer of the olfactory bulb V u cuneate nucleus of the ventral telencephalon GL glomerular layer of the olfactory bulb Vv ventral nucleus of the ventral telencephalon the correlation between the size of the dorsolateral telen- (the serranid Serranus scriba [Rakic and Lazarevic, 1977]; cephalon in two blenniids and their home range provided two centrarchids, Lepomis cyanellus [Northcutt and Da- some functional evidence for the proposed homology be- vis, 1983] and Lepomis gibbosus [Fortuyn, 1961]; the os- tween the dorsolateral telencephalon of fishes and the phronemid Betta splendens [Marino-Neto and Sabbatini, hippocampus of mammals [Costa et al., 2011]. If clear 1988]; the moronid Dicentrarchus labrax [Cerdá-Revert- phylogenetic relationships exist, we can compare the neu- er et al., 2001]; the sparid Sparus aurata [Muñoz-Cueto roanatomical features of different species in order to de- et al., 2001]; the channid Channa gachua [Baile and Patle, velop hypotheses about the selection pressures which 2011], and a single cichlid, Astatotilapia burtoni [Bur- shape neural circuits of behavior. Perciform fishes are the meister et al., 2009]). Detailed descriptions of the telen- most speciose and behaviorally diverse order of verte- cephalon of behaviorally diverse basal and derived species brates. This makes them an ideal group to identify behav- are important for the development of hypotheses relevant iorally relevant circuits as well as evolutionary processes to brain evolution, neural development, comparative that might shape brain function. However, one key im- function and proximate mechanisms of behavior [Bra- pediment is that the cytoarchitecture of the perciform fish ford, 2009]. For example, Demski and Beaver [2001] sur- telencephalon is only described in detail for a few species veyed the organization of the telencephalon in multiple 32 Brain Behav Evol 2014;84:31–50 Dewan /Tricas DOI: 10.1159/000363124 Downloaded by: University of Hawaii Library 128.171.57.189 - 9/12/2014 7:50:07 PM species within the Beryciformes, Perciformes and Tetra- rological studies across butterflyfishes. In addition, since odontiformes orders. The results of that study highlight- C. multicinctus differs from many other species examined ed three brain regions within the dorsal telencephalon in terms of their mating system, feeding guild and habitat, (the dorsal part of the lateral zone, the medial zone and hypotheses relevant to perciform fish brain function can the central zone) that were hypertrophied in reef fishes. be proposed. While this comparative work proposed several interest- ing and important hypotheses, it did not offer detailed descriptions of the entire telencephalon of these species. Materials and Methods Thus, further studies which characterize the entire telen- cephalon in perciform fishes, particularly from species Animals with well-described social behaviors and those that live in Thirty-two adult male (n = 15) and female (n = 17) C. multi- complex environments such as coral reefs, are needed. cinctus were collected with barrier and hand nets from the west and north shore of Oahu (Hawaii, USA). Fish were housed overnight The spatially complex environment and high biodiver- at the Hawai’i Institute of Marine Biology in flow-through saltwa- sity on coral reefs are evident in the large number of eco- ter tanks prior to analysis. The original research reported herein logical niches filled by perciform fishes. The evolution of was performed under the Institutional Animal Care and Use Com- the diverse social behavior and feeding guilds that are ap- mittee guidelines for vertebrate care and use established by the parent on coral reefs may be associated with concurrent University of Hawai’i. changes within the brain. However, to date, there has Histology been no detailed neuroanatomical study in a fish which Adult male (n = 4) and female (n = 4) fish were anesthetized with exclusively inhabits coral reefs, although
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