Oxytocin (OT) mediates social habituation in rodent model systems, but its role in mediating this effect in other vertebrates is unknown. We used males of the African cichlid fish, Astatotilapia burtoni, to investigate two aspects of isotocin (IT; an OT homolog) signaling in social habituation. First, we examined the expression of IT receptor 2 (ITR2) as well as two immediate early genes in brain regions implicated in social recognition. Next, we examined IT neuron activity using immunohistochemistry. Patterns of gene expression in homologs of the amygdala and hippocampus implicate IT signaling in these regions in social habituation to a territorial neighbor. In the preoptic area, the expression of the ITR2 subtype and IT neuron activity respond to the presence of a male, independent of familiarity. Our results implicate IT in mediating social habituation in a teleost.

Keywords:
Hippocampus, Preoptic area, Immediate early genes, Social bonding, Social habituation, Gene expression, Teleost
1.
Adolphs R (2010): What does the amygdala contribute to social cognition? Ann NY Acad Sci 1191:42-61.
2.
Bale TL, Davis AM, Auger AP, Dorsa DM, McCarthy MM (2001): CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J Neurosci 21:2546-2552.
3.
Bee MA, Gerhardt HC (2001): Habituation as a mechanism of reduced aggression between neighboring territorial male bullfrogs (Rana catesbeiana). J Comp Psychol 115:68-82.
4.
Beery AK, Zucker I (2010): Oxytocin and same-sex social behavior in female meadow voles. Neuroscience 169:665-673.
5.
Benjamini Y, Hochberg Y (1995): Controlling the false discovery rate: a practical and powerful approach to multiple testing.. J R Stat Soc B 7:289-300.
6.
Blumstein DT, Daniel JC (2007): Quantifying Behavior the JWatcher Way. Sunderland, Sinauer Associates.
7.
Choleris E, Kavaliers M, Pfaff DW (2004): Functional genomics of social recognition. J Neuroendocrinol 16:383-389.
8.
Choleris E, Ogawa S, Kavaliers M, Gustafsson J-A, Korach KS, Muglia LJ, et al (2006): Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice. Genes Brain Behav 5:528-539.
9.
Crockford C, Wittig RM, Langergraber K, Ziegler TE, Zuberbühler K, Deschner T (2013): Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proc Biol Sci 280:20122765.
10.
De Dreu CKW (2012): Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda. Horm Behav 61:419-428.
11.
Demski LS (2013): The pallium and mind/behavior relationships in teleost fishes. Brain Behav Evol 82:31-44.
12.
Desjardins JK, Klausner JQ, Fernald RD (2010): Female genomic response to mate information. Proc Natl Acad Sci USA 107:21176-21180.
13.
Donaldson ZR, Young LJ (2008): Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900-904.
14.
Ebitz RB, Platt ML (2014): An evolutionary perspective on the behavioral consequences of exogenous oxytocin application. Front Behav Neurosci 7:225.
15.
Ebitz RB, Watson KK, Platt ML (2013): Oxytocin blunts social vigilance in the rhesus macaque. Proc Natl Acad Sci USA 110:11630-11635.
16.
Ferguson JN, Aldag JM, Insel TR, Young LJ (2001): Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21:8278-8285.
17.
Fernald RD, Maruska KP (2012): Social information changes the brain. Proc Natl Acad Sci USA 109:17194-17199.
18.
Getty T (1987): Dear enemies and the prisoner's dilemma: why should territorial neighbors form defensive coalitions? Integr Comp Biol 27:327-336.
19.
Gheusi G, Bluthé R-M, Goodall G, Dantzer R (1994): Social and individual recognition in rodents: methodological aspects and neurobiological bases. Behav Processes 33:59-87.
20.
Godwin J, Thompson R (2012): Nonapeptides and social behavior in fishes. Horm Behav 61:230-238.
21.
Gordon I, Zagoory-Sharon O, Leckman JF, Feldman R (2010): Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood. Horm Behav 58:513-518.
22.
Grosenick L, Clement TS, Fernald RD (2007): Fish can infer social rank by observation alone. Nature 445:429-432.
23.
Gur R, Tendler A, Wagner S (2014): Long-term social recognition memory is mediated by oxytocin-dependent synaptic plasticity in the medial amygdala. Biol Psychiatry 76:377-386.
24.
Harvey-Girard E, Tweedle J, Ironstone J, Cuddy M, Ellis W, Maler L (2010): Long-term recognition memory of individual conspecifics is associated with telencephalic expression of Egr-1 in the electric fish Apteronotus leptorhynchus. J Comp Neurol 518:2666-2692.
25.
Herdegen T, Leah JD (1998): Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Rev 28:370-490.
26.
Heyes CM (1994): Social learning in animals: categories and mechanisms. Biol Rev 69:207-231.
27.
Hofmann HA (2003): Functional genomics of neural and behavioral plasticity. J Neurobiol 54:272-282.
28.
Huffman LS, O'Connell LA, Kenkel CD, Kline RJ, Khan IA, Hofmann HA (2012): Distribution of nonapeptide systems in the forebrain of an African cichlid fish, Astatotilapia burtoni. J Chem Neuroanat 44:86-97.
29.
Hurlemann R, Patin A, Onur OA, Cohen MX, Baumgartner T, Metzler S, et al. (2010): Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J Neurosci 30:4999-5007.
30.
Johnson ZV, Young LJ (2015): Neurobiological mechanisms of social attachment and pair bonding. Curr Opin Behav Sci 3:38-44.
31.
Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, et al (2001): A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289-296.
32.
Kidd MR, Dijkstra PD, Alcott C, Lavee D, Ma J, O'Connell LA, et al (2013): Prostaglandin F2α facilitates female mating behavior based on male performance. Behav Ecol Sociobiol 67:1307-1315.
33.
Klatt JD, Goodson JL (2013): Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird. Proc Biol Sci 280:20122396.
34.
Lee H-J, Macbeth AH, Pagani JH, Young WS (2009): Oxytocin: the great facilitator of life. Prog Neurobiol 88:127-151.
35.
Livak KJ, Schmittgen TD (2001): Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method. Methods 25:402-408.
36.
Matz MV, Wright RM, Scott JG (2013): No control genes required: Bayesian analysis of qRT-PCR data. PLoS One 8:e71448.
37.
Maximino C, Lima MG, Oliveira KRM, Batista E de JO, Herculano AM (2013): “Limbic associative” and “autonomic” amygdala in teleosts: a review of the evidence. J Chem Neuroanat 48-49:1-13.
38.
Mello C, Nottebohm F, Clayton D (1995): Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon. J Neurosci 15:6919-6925.
39.
Meyer A, Van de Peer Y (2005): From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937-945.
40.
Ocampo Daza D, Lewicka M, Larhammar D (2012): The oxytocin/vasopressin receptor family has at least five members in the gnathostome lineage, inclucing two distinct V2 subtypes. Gen Comp Endocrinol 175:135-143.
41.
O'Connell LA, Hofmann HA (2011): The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599-3639.
42.
O'Connell LA, Matthews BJ, Hofmann HA (2012): Isotocin regulates paternal care in a monogamous cichlid fish. Horm Behav 61:725-733.
43.
O'Connell LA, Rigney MM, Dykstra DW, Hofmann HA (2013): Neuroendocrine mechanisms underlying sensory integration of social signals. J Neuroendocrinol 25:644-654.
44.
O'Connor CM, Marsh-Rollo SE, Ghio SC, Balshine S, Aubin-Horth N (2015): Is there convergence in the molecular pathways underlying the repeated evolution of sociality in African cichlids? Horm Behav 75:160-168.
45.
Ophir AG, Zheng D-J, Eans S, Phelps SM (2009): Social investigation in a memory task relates to natural variation in septal expression of oxytocin receptor and vasopressin receptor 1a in prairie voles (Microtus ochrogaster). Behav Neurosci 123:979-991.
46.
Owen PC, Perrill SA (1998): Habituation in the green frog, Rana clamitans. Behav Ecol Sociobiol 44:209-213.
47.
Peeke HV, Peeke SC (1973): Habituation in fish with special reference to intraspecific aggressive behavior; in Peeke HV, Herz MJ (eds): Habituation. New York, Academic Press, pp 59-83.
48.
Popik P, van Ree JM (1991): Oxytocin but not vasopressin facilities social recognition following injection into the medial preoptic area of the rat brain. Eur Neuropsychopharmacol 1:555-560.
49.
Portavella M, Torres B, Salas C (2004a): Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24:2335-2342.
50.
Portavella M, Torres B, Salas C, Papini MR (2004b): Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratu s). Neurosci Lett 362:75-78.
51.
Rilling JK, DeMarco AC, Hackett PD, Thompson R, Ditzen B, Patel R, et al (2012): Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology 37:447-461.
52.
Romero T, Nagasawa M, Mogi K, Hasegawa T, Kikusui T (2014): Oxytocin promotes social bonding in dogs. Proc Natl Acad Sci USA 111:9085-9090.
53.
Spreng RN, Mar RA (2012): I remember you: a role for memory in social cognition and the functional neuroanatomy of their interaction. Brain Res 1428:43-50.
54.
Swanson LW, Petrovich GD (1998): What is the amygdala? Trends Neurosci 21:323-331.
55.
Temeles EJ (1994): The role of neighbours in territorial systems: when are they “dear enemies”? Anim Behav 47:339-350.
56.
Tessmar-Raible K, Raible F, Christodoulou F, Guy K, Rembold M, Hausen H, et al (2007): Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129:1389-1400.
57.
Tischmeyer W, Grimm R (1999): Activation of immediate early genes and memory formation. Cell Mol Life Sci 55:564-574.
58.
Weitekamp CA, Hofmann HA (2017): Neuromolecular correlates of cooperation and conflict during territory defense in a cichlid fish. Horm Behav 89:145-156.
59.
Weitekamp CA, Nguyen J, Hofmann HA (2017): Social context affects behavior, preoptic area gene expression, and response to D2 receptor manipulation during territorial defense in a cichlid fish. Genes Brain Behav, in press.
© 2017 S. Karger AG, Basel
2017
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.