Neural Circuit Reconfiguration by Social Status

The social rank of an animal is distinguished by its behavior relative to others in its community. Although social-status-dependent differences in behavior must arise because of differences in neural function, status-dependent differences in the underlying neural circuitry have only begun to be described. We report that dominant and subordinate crayfish differ in their behavioral orienting response to an unexpected unilateral touch, and that these differences correlate with functional differences in local neural circuits that mediate the responses. The behavioral differences correlate with simultaneously recorded differences in leg depressor muscle EMGs and with differences in the responses of depressor motor neurons recorded in reduced, in vitro preparations from the same animals. The responses of local serotonergic interneurons to unilateral stimuli displayed the same status-dependent differences as the depressor motor neurons. These results indicate that the circuits and their intrinsic serotonergic modulatory components are configured differently according to social status, and that these differences do not depend on a continuous descending signal from higher centers.

[1]  Jan-Marino Ramirez,et al.  Network reconfiguration and neuronal plasticity in rhythm-generating networks. , 2011, Integrative and comparative biology.

[2]  L. O’Connell,et al.  Genes, hormones, and circuits: An integrative approach to study the evolution of social behavior , 2011, Frontiers in Neuroendocrinology.

[3]  T. Preuss,et al.  Serotonergic modulation of startle-escape plasticity in an African cichlid fish: a single-cell molecular and physiological analysis of a vital neural circuit. , 2011, Journal of neurophysiology.

[4]  Fadi A. Issa,et al.  Neural circuit activity in freely behaving zebrafish (Danio rerio) , 2011, Journal of Experimental Biology.

[5]  T. Preuss,et al.  Social and ecological regulation of a decision-making circuit. , 2010, Journal of neurophysiology.

[6]  H. Albers,et al.  Arginine‐vasopressin and the regulation of aggression in female Syrian hamsters (Mesocricetus auratus) , 2010, The European journal of neuroscience.

[7]  Daniel Cattaert,et al.  Social Interactions Determine Postural Network Sensitivity to 5-HT , 2010, The Journal of Neuroscience.

[8]  G. Robinson,et al.  Genes and Social Behavior , 2008, Science.

[9]  D. H. Edwards,et al.  Conservation of structure, signaling and pharmacology between two serotonin receptor subtypes from decapod crustaceans, Panulirus interruptus and Procambarus clarkii , 2008, Journal of Experimental Biology.

[10]  Robert J Calin-Jageman,et al.  Parameter space analysis suggests multi-site plasticity contributes to motor pattern initiation in Tritonia. , 2007, Journal of neurophysiology.

[11]  D. H. Edwards,et al.  Direct Benefits of Social Dominance in Juvenile Crayfish , 2007, The Biological Bulletin.

[12]  Cynthia L. Jordan,et al.  Social control of brain morphology in a eusocial mammal , 2007, Proceedings of the National Academy of Sciences.

[13]  D. H. Edwards,et al.  Social domination increases neuronal survival in the brain of juvenile crayfish Procambarus clarkii , 2007, Journal of Experimental Biology.

[14]  Russell D. Fernald,et al.  Social dominance regulates androgen and estrogen receptor gene expression , 2007, Hormones and Behavior.

[15]  T. Jones,et al.  Developmental and dominance‐associated differences in mushroom body structure in the paper wasp Mischocyttarus mastigophorus , 2007, Developmental neurobiology.

[16]  D. H. Edwards,et al.  The effects of social experience on the behavioral response to unexpected touch in crayfish , 2006, Journal of Experimental Biology.

[17]  Donald H Edwards,et al.  Immunocytochemical mapping and quantification of expression of a putative type 1 serotonin receptor in the crayfish nervous system , 2005, The Journal of comparative neurology.

[18]  E. Gould,et al.  Dominance Hierarchy Influences Adult Neurogenesis in the Dentate Gyrus , 2004, The Journal of Neuroscience.

[19]  B. Antonsen,et al.  Differential dye coupling reveals lateral giant escape circuit in crayfish , 2003, The Journal of comparative neurology.

[20]  Fadi A. Issa,et al.  The neural basis of dominance hierarchy formation in crayfish , 2003, Microscopy research and technique.

[21]  R. Fernald Social regulation of the brain: sex, size and status. , 2008, Novartis Foundation symposium.

[22]  D. H. Edwards,et al.  Metamodulation of the Crayfish Escape Circuit , 2003, Brain, Behavior and Evolution.

[23]  S. White,et al.  Social regulation of gonadotropin-releasing hormone. , 2002, The Journal of experimental biology.

[24]  R. Keller,et al.  The eyestalk-androgenic gland-testis endocrine axis in the crayfish Cherax quadricarinatus. , 2002, General and comparative endocrinology.

[25]  Fadi A. Issa,et al.  Patterns of Neural Circuit Activation and Behavior during Dominance Hierarchy Formation in Freely Behaving Crayfish , 2001, The Journal of Neuroscience.

[26]  Fadi A. Issa,et al.  Dominance hierarchy formation in juvenile crayfish procambarus clarkii , 1999, The Journal of experimental biology.

[27]  D. H. Edwards,et al.  Metamodulation: the control and modulation of neuromodulation , 1999 .

[28]  E. Kravitz,et al.  Autoinhibition of serotonin cells: an intrinsic regulatory mechanism sensitive to the pattern of usage of the cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  F. Krasne,et al.  Altered Excitability of the Crayfish Lateral Giant Escape Reflex during Agonistic Encounters , 1997, The Journal of Neuroscience.

[30]  S R Yeh,et al.  Neuronal Adaptations to Changes in the Social Dominance Status of Crayfish , 1997, The Journal of Neuroscience.

[31]  D. H. Edwards,et al.  The Effect of Social Experience on Serotonergic Modulation of the Escape Circuit of Crayfish , 1996, Science.

[32]  Christiane Rossi-Durand,et al.  Peripheral proprioceptive modulation in crayfish walking leg by serotonin , 1993, Brain Research.

[33]  Mapping of serotonin-like immunoreactivity in the ventral nerve cord of crayfish , 1990, Brain Research.

[34]  Newton H. Copp,et al.  DOMINANCE HIERARCHIES IN THE CRAYFISH PROCAMBARUS CLARKII (GIRARD, 1852) AND THE QUESTION OF LEARNED INDIVIDUAL RECOGNITION (DECAPODA, ASTACIDEA) , 1986 .

[35]  E. Kravitz,et al.  Mapping of serotonin-like immunoreactivity in the lobster nervous system , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.