Richmond Thompson

Professor of Psychology and Neuroscience

On leave for 2017-18 academic year

Work in my lab explores how steroid hormones and neuropeptides in the vasopressin / oxytocin family influence social behavior in vertebrates. Primarily, we want to learn how and where within the brain these molecules act to influence interactions between individuals, particularly in reproductive contexts. Although I have worked with numerous species across broad vertebrate groups, current work focuses on goldfish and zebrafish, two closely related, highly social teleosts. We examine the molecular and cellular mechanisms through which androgens and estrogens, as well as the neuropeptide vasotocin, affect behavioral and brain responses to sensory cues that elicit different types of social output, from courtship to aggression to withdrawal. More specifically, we are investigating the mechanisms through which testosterone and estradiol rapidly modulate early stages of visual and olfactory sensory processing. We are also characterizing the neural circuits through which vasotocin, the ancestral homologue of vasopressin, promotes context-dependent social withdrawal in male goldfish, as well as the receptor mechanisms that underlie its ability to have different behavioral effects in different social contexts. A complimentary line of research explores how vasopressin modulates social perceptions in humans, and through a collaboration with a colleague at Emory University, where within our own brains it produces such influences.

Ultimately, we hope to:

  1. characterize steroid and neuropeptide mechanisms that evolved to help different species solve social challenges associated with their unique life histories, and
  2. identify molecular, cellular, and anatomical similarities in how these molecules work across species that represent the fundamental principles through which brain neurochemistry affects social behavior in vertebrates.

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Education

  • BS, Biology, Psychology double major, Furman University, 1989
  • PhD, Biopsychology, Cornell University, 1996
  • Postdoctoral Experience: Zoology Dept, Oregon State, 1996-1999

PDF Curriculum Vitae

The Thompson Lab

Although there is obvious variation in brain organization across vertebrate species, the basic brain blueprint has remained remarkably stable for millions of years, as have the mechanistic principles associated with how it regulates various functions, including behavior. That conservation includes the presence of common circuits across vertebrates that are critical for social regulation. In my lab, we explore the molecular, cellular, and behavioral mechanisms through which two types of molecules, sex steroids and neuropeptides in the vasopressin/oxytocin family, act within those circuits to influence social behaviors associated with reproduction.

Non-genomic Sex Steroid Mechanisms and Social Regulation

Immunohistochemical labeling of GPR30, a membrane estrogen receptor (red) and the peptide isotocin (green) showing that the same cells in the preoptic area make both molecules.
Immunohistochemical labeling of GPR30, a membrane estrogen receptor (red) and the peptide isotocin (green) showing that the same cells in the preoptic area make both molecules.

We know a great deal about the genomic mechanisms through which androgens and estrogens influence behavior; by turning genes on and off and thus affecting levels of proteins in cells, they slowly sculpt the brain circuits and peripheral structures required to produce social output. However, we now recognize that steroids can also rapidly modulate how those circuits respond to social stimuli by acting on receptors on neuronal membranes, a non-genomic mechanism. Steroids thus play dynamic roles in social regulation. We are currently trying to identify the membrane receptors that mediate rapid effects of androgens and estrogens on behavioral and physiological processes related to courtship in goldfish, as well as to determine if these steroids rapidly affect early stages of sensory processing in ways that amplify neural responses to social stimuli. We are also beginning to explore if sex steroids have similar, rapid effects in closely related zebrafish. If so, we will be able to take advantage of the genetic tools developed in that species to increase the resolution with which we can examine non-genomic steroid mechanisms.

Nonapeptides and Socialiality

We can directly infuse chemicals into the brain through surgically implanted cannula to test their effects on social approach behavior.

In vertebrates, 9-amino acid containing peptides in the vasopressin/oxytocin family all evolved from a common ancestral molecule, vasotocin, in which a gene mutation gave rise to the mammalian homologue, vasopressin. Gene duplications and subsequent mutations also led to the evolution of numerous sister nonapeptides across vertebrates, including isotocin in teleost fish and oxytocin in mammals. All are structurally similar, produced in the brain, and play important roles in social regulation across vertebrates, though they can influence behavior differently depending on the species, sex and social context. In reproductive contexts in male goldfish, vasotocin inhibits approach responses towards other males, but not towards ovulating females. We have characterized the circuit that mediates its ability to promote social withdrawal, and we are now exploring the mechanisms that turn that circuit off when males interact with females. Specifically, we are exploring the possibility that unique social cues differentially regulate expression of the gene for the vasotocin receptor and/or for related proteins that may dimerize with the receptor and thus modulate its binding and/or cell signaling properties, either of which could change the peptide’s behavioral effects across social contexts.

We are also exploring how intranasal vasopressin, which crosses the blood brain barrier in humans, influences subjective responses to faces in men and women and, through a collaboration with James Rilling at Emory University, how vasopressin modulates brain responses to those stimuli. These studies have indicated that, as in other vertebrates, vasopressin’s social effects in humans are sex-specific and differ as a function of social context. They have also suggested that a single, intranasal dose of vasopressin may produce lasting effects on some social responses.

Recent Student Honors Projects in the Thompson Lab

  • Does vasotocin produce a context dependent effect in male Carassius auratus: testing its effects on male courtship? Christine Andersen, 2017
  • Rapid effects of estrogens on visual processing in male goldfish, Carassius auratus. Nicole Sekula, 2017.
  • Investigating the effects of sex steroids in the optic tectum in common goldfish, Carassius auratus. Felice Chan, 2017

Publications

Yue, S,* Wadia, V,* Sekula, N,* Dickinson, PS, Thompson, RR (2017). Acute effects of sex steroids on visual processing in male goldfish, Carraisus auratus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol

Price, D, Burris, D, Coultier, A, Thompson, CA, Rilling, JK, Thompson, RR (2017) Dose-dependent and lasting effects of intranasal vasopressin on face processing in men. Frontiers in Endocrinology

Rilling, JK, Li, T, Chen, X, Guatam, P, Haroon, E., Thompson, RR (2017) Arginine vasopressin effects on subjective and neural responses to same- and other-sex faces in men and women. Frontiers in Endocrinology, Aug 21;8:200

Mangiamele LA,+ Gomez JR,* Curtis NJ, Thompson RR (2017). GPER/GPR30, a membraneestrogen receptor, is expressed in the brain and retina of a social fish (Carassius auratus) and colocalizes with isotocin. J Comp Neurol. 525; 252-270

Rilling JK, Demarco AC, Hackett PD, Chen X, Gautam P, Stair S, Haroon E, Thompson R, Ditzen B, Patel R, Pagnoni G. (2014) Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction. Psychoneuroendocrinology, 39:237-48

Thompson, RR, Walton, JC (2013) Social regulatory functions of vasotocin and isotocin in fish. In Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior, pp 75-104. Cambridge University Press, eds Choleris, Pfaff, Kaveliers.

Mangiamele, L,+ Keeney,* A., D’Agostino, E.,* ; Thompson, RR (2013) Pheromone exposure influences preoptic arginine vasotocin gene expression and inhibits social approach behavior in response to rivals, but not potential mates. Brain Behavior Evolution, 81, 194-202

Goodson, JL., Kelly, Kingsbury, MA, Thompson, RR (2012) An aggressive-specific cell type in the anterior hypothalamus of finches. Proceedings of the National Academy of Science, USA, 109(34):13847-52

Thompson, RR, Mangiamele+, L+ (2012) Rapid effects of estradiol on behavioral and physiological responses related to reproduction in male goldfish. In Brain Aromatase, Estrogens, and Behavior, eds Balthazart and Ball, Oxford Press.

Mangiamele+, L,+ Thompson, RR (2012) Testosterone rapidly stimulates ejaculate volume and sperm density through an estrogenic membrane receptor mechanism in a competitive breeding fish. Hormones and Behavior Jul;62(2):107-12

Godwin, J., Thompson RR (2012) Nonapeptides and social behavior in fish. Hormones and Behavior 61, 230-238

Rilling, J, DeMarco, A., Hackett, P, Thompson, R, Sitzen, B, Patel, R, Pagnon, G. (2012) Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity. Psychoneuroendocrinology 37; 437-461.

Kelley, A, Kingsbury, M., Hofbuhr, K., Schrock, S., Waxman, B*, Kabelik, D., Thompson, R, Goodson, J. (2011) Extended amygdala nonapeptide neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty. Hormones and Behavior, 60, 12-21.

Searcy, B, Bradford, S, Thompson, RR, Fitz, TM, Moore, FL (2011). Identifiication and characterization of mesotocin and V1a-like receptors in a urodele amphibian, Taricha granulosa. General and Comparative Endocrinology 170; 131-143.

Goodson, JL and Thompson, RR (2010). Nonapeptide mechanisms of social cognition, behavior, and species-specific social sytems. Current Opinions in Neurobiology 20; 784-794

Walton JC, Waxman B*, Hoffbuhr K, Kennedy M*, Beth E*, Scangos J*, Thompson RR. (2010) Behavioral effects of hindbrain vasotocin in goldfish are seasonally variable but not sexually dimorphic. Neuropharmacology 58(1) 126-134.

Lord, LD*, Bond, J.*, Thompson, RR. (2009) Rapid steroid influences on visually-guided sexual behavior in goldfish. Hormones and Behavior 56(5) 519-526.

Thompson, RR Walton, JC (2009) Vasotocin immunoreactivity in goldfish brains characterizing primitive circuits associated with social regulation. Brain Behavior and Evolution, 73(3) 153-164.

Searcy, B., Walthers, EA, Heppner, BL, Thompson, RR, Moore, FL. (2009) Identification of mesotocin and vasotocin nucleotide sequences in two species of urodele amphibian. General and Comparative Endocrinology, 160(2):111-6.

Thompson, RR, Dickinson, PS, Rose, JL, Dakin, K*, Civiello, G*, Segerdahl, A*, and Bartlett, R*. (2008) Pheromones enhance somatosensory processing in newt brains through a vasotocin-dependent mechanism. Proceedings of the Royal Society, Biological Sciences, UK, 275(1643); 1685-1693.

Thompson, RR, Walton, JC, Bhalla, R,* George, KC,* Beth, EC.* (2008) A primitive social circuit: vastocin-substance P interactions in the hindbrain influence social behavior through a peripheral feedback mechanism. European Journal of Neuroscience, 27(9); 2285-2293.

Thompson RR, George K, Walton JC, Orr SP, Benson J. (2006) Sex-specific influences of vasopressin on human social communication. Proceedings of the National Academy of Science USA. May 16: 103(20) 7889-94.

Thompson, RR, George, K,* Dempsey, J,* Walton, JE. (2004) Visual sex discrimination in goldfish: seasonal, sexual and androgenic influences. Hormones and Behavior, 46(5):646-54.

Thompson, RR Walton, JC. (2004). Peptide effects on social behavior: the effects of vasotocin and isotocin on social approach behavior in male goldfish. Behavioral Neuroscience, 118(3), 620-626.

Thompson, RR, Gupta, S.,* Miller, K, Mills, S, Orr, S. (2004). Vasopressin effects on facial responses related to social communication in human males. Psychoneuroendocrinology, 29, 35-48.

Thompson, RR Moore, FL. (2003) The effects of testosterone and vasotocin on behavioral responses to visual and olfactory female sexual stimuli in ovariectomized female roughskin newts. Hormones and Behavior, 44, 311-318.

Thompson, RR. George, K.* (2003) Testing the relationship between endogenous testosterone and physiological responses to facial stimuli in human males: an experiment conducted in an undergraduate behavioral neuroscience laboratory course. Journal of Undergraduate Neuroscience Research, 1.

Thompson, R. Moore, F. (2000) Vasotocin stimulates appetitive behavioral responses to the visual and olfactory stimuli used by male roughskin newts during courtship. Hormones and Behavior, 38, 75-85.

Thompson, RR, Tokar, Z,* Pistohl, D* Moore, FL. (1999) Behavioral evidence for a sex-pheremone in roughskin newts, Taricha granulosa. In Advances in Chemical Signals in Vertebrates, ed. By R.E. Johnston, D. Muller-Schwartze, and P. Sorenson, pp 421-430, Plenum Press, New York.

Thompson, RR, Goodson, JL, Ruscio, MG. Adkins-Regan, E. (1998) Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail, (Coturnix japonica) : a comparison of function with the medial nucleus of the amygdala in mammals. Brain Behavior Evolution, 51, 215-229.

Adkins-Regan, E, Mansukani, V, Thompson, R. Yang, S. (1997) Organizational effects of sex hormones on sexual partner preferences in zebra finches. Brain Research Bulletin., 44(4), 497-502.

Goodson, JL, Eibach, R, Dukes, A, Friedman, M, Sakata, J, Thompson, RR Adkins-Regan E. (1997) Neurobiology of social organization. Effects of lateral septum lesions in a territorial songbird, the field sparrow (Spizella pusilla), and a colonial songbird, the zebra finch. Ann. N.Y. Acad. Sci., 807, 518-521.

Thompson, RR, Adkins-Regan, E. (1994) Photoperiod affects the morphology of a sexually dimorphic nucleus in the preoptic area of Japanese quail, Coturnix japonica. Brain Research, 667, 201-208.

Adkins-Regan, E, Mansukani, V., Seiwert, C. Thompson, R. (1994) Sexual differentiation of brain and behavior in zebra finches. Journal Neurobiology, 15, 868-877.

Other Interests

Professor Thompson fly fishing in a river.

Rick enjoys the wonderful outdoor opportunities in Maine, particularly fly fishing for trout in the north and striper on the ocean.