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My research focuses on understanding the neural circuitry that underlies different maternal behaviors in rodents. In a wide range of mammals, including primates, bears, cats, dogs and mice, mothers are highly protective when their offspring are young and vulnerable. As part of this protective behavior, lactating females will attack a threat against their offspring in a behavior termed maternal aggression or maternal defense. Although offspring protection plays a critical role in the perpetuation of species and offspring, it has received relatively little research attention. The present focus of my lab work is understanding the genetic, hormonal, and neural basis of maternal defense behavior. I am also interested in examining the neuroendocrine basis of other maternal behaviors, such as elevated arousal, nursing, pup retrieval, and licking and grooming of pups. A recent development in the lab has been characterizing naturally occurring maternal neglect that occurs in a mouse model in our lab. Researchers in my lab will be given the opportunity to participate in on-going studies and/or initiate independent projects.

The general approach in the laboratory is to use multiple levels of analysis to gain insights into how neural circuitry controls behavior. The techniques used in the lab include behavioral testing, immunohistochemistry, direct testing of neuromodulators on behavior (via cannula implanted in the CNS), pharmacological techniques, anatomical techniques, Western blotting, and analysis of gene expression in subregions of the brain using gene arrays and real-time PCR. Studies are conducted on mice, including knockout mice.

We previously have examined the role for corticotropin releasing factor (CRF) and its related peptides, urocortin (Ucn) 1, and Ucn 3 in the regulation of maternal defense. Results from these and other studies have consistently highlighted a role of lateral septum (LS) in regulating offspring protection. We currently are focusing on GABA and norepinephrine (NE) signaling in LS as a key mechanism for regulating maternal defense. As shown below, LS is highly connected with other regions regulating offspring protection.

We have two novel lines of mice in our lab. One line has very high levels of maternal defense and we derived this line from outbred mice using an artificial selection approach. We use this line for most of our offspring protection studies. A second line of mice also has high maternal defense, but was originally a mouse line selected for high wheel running. We identified high offspring protection in this line and while maintaining it in our lab realized that high rates of naturally occurring maternal neglect appeared each generation. Thus, we now maintain this line for studies on the neural and genetic basis of maternal neglect.

As part of our selection study for high maternal defense, we examined gene expression changes (using gene array analysis) that occurred in the CNS in association with high offspring protection. We are currently following up on some of these findings and are examining roles for neurotensin and CRF binding protein in maternal defense.

Pheromonal activation of vomeronasal organ leads to activation of the accessory olfactory bulb that then may help trigger maternal defense. The lab is currently examining brain activity changes in association with aggression in mice either with or without a functional pheromonal response (missing the trp2 channel).

This schematic diagram is developed from a wide range of studies using multiple approaches and highlights LS as a critical node in the regulation of offspring protection.

Prospective graduate students and postdoctoral fellows should send me a letter or E-mail of inquiry including areas of interest and relevant experience. Prospective graduate students can gain access to my lab through either the Department of Zoology (Madison) or Neuroscience Training Program (Madison) at the University of Wisconsin.

Nina S. Hasen Ph.D. (2007); B.A. from Oberlin College
Kimberly L. D'Anna Ph.D. (2008); B.S. from Michigan State University

Gammie SC, Edelmann MN, Mandel-Brehm C, D’Anna KL, Auger AP, Stevenson SA (2008). Altered dopamine signaling in naturally occurring maternal neglect. Public Library of Science ONE, 1:e1974. (open access)

Gammie SC, Auger AP, Jessen HM, Vanzo RJ, Awad TA, Stevenson SA (2007). Altered gene expression in mice selected for high maternal aggression. Genes, Brain and Behavior, 6:432-43. (open access)

Lee G, Gammie SC (2007). GABA enhancement of maternal defense in mice: possible neural correlates. Pharmacology, Biochemistry and Behavior, 86:176-87. (open access)

Gammie SC, Bethea ED, Stevenson SA (2007). Altered maternal profiles in corticotropin-releasing factor receptor 1 deficient mice. BMC Neuroscience, 8:17. (open access)

D’Anna KD, Gammie SC (2006). Hypocretin-1 dose-dependently modulates maternal behaviour in mice. Journal of Neuroendocrinology, 18:553-566. (open access)

Gammie SC, Stevenson SA (2006). Effects of daily and acute restraint stress during lactation on maternal aggression and behavior in mice. Stress, 9:171-180.

Hasen, NS, Gammie SC (2006). Maternal aggression: new insights from Egr-1. Brain Research, 1108:147-156.

Gammie SC, Garland T, Stevenson SA (2006). Artificial selection for increased maternal defense behavior in mice. Behavior Genetics, 36:713-722.

Gammie SC, Stevenson SA (2006). Intermale aggression in corticotropin-releasing factor receptor 1 deficient mice. Behavioural Brain Research, 171:63-69.

Gammie SC (2005). Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behavioral and Cognitive Neuroscience Reviews, 4:119-135.

Gammie SC, Hasen NS Awad TA, Auger AP, Jessen HM, Panksepp JB, Bronikowski AM (2005). Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice. Brain Research. Molecular Brain Research, 139:201-211. (open access)

D’Anna KL, Stevenson SA, Gammie SC (2005). Urocortin 1 and 3 impair maternal maternal defense behavior in mice. Behavioral Neuroscience, 119:1061-1071.

Friske JE, Gammie SC (2005). Environmental enrichment alters plus maze, but not maternal defense performance in mice. Physiology and Behavior, 85:187-194.

Hasen NS, Gammie SC (2005). Differential fos activation in virgin and lactating mice in response to an intruder. Physiology and Behavior, 84:681-695.

Gammie SC, Hasen NS, Stevenson SA, Bale TL, D’Anna KL (2005). Elevated stress sensitivity in corticotropin-releasing factor receptor 2 deficient mice decreases maternal, but not intermale aggression. Behavioural Brain Research, 160:169-177.

Rhodes JS, Gammie SC, Garland T (2005). Neurobiology of mice selected for high voluntary wheel-running activity. Integrative and Comparative Biology, 45:438-455.

Gammie SC, Nelson RJ (2005). High maternal aggression in dwarf hamsters (Phodopus campbelli and P. sungorus). Aggressive Behavior, 31:294-302.

Smith GT, Allen AR, Oestreich J, Gammie SC (2005). L-citrulline immunoreactivity reveals nitric oxide production in the electromotor and electrosensory systems of the weakly electric fish, Apteronotus leptorhynchus. Brain, Behavior, and Evolution, 65:1-13.

Gammie SC, Lonstein JS (2005). Maternal aggression. In: Biology of Aggression. R. J. Nelson (editor). Oxford University Press, New York, NY.

Bronikowski AM, Rhodes JS, Garland T, Prolla T, Awad T, Gammie SC (2004). The evolution of gene expression in the hippocampus in response to selection for increased locomotor activity. Evolution, 58:2079-2086.

Gammie SC, Negron A, Newman SM, Rhodes JS (2004). Corticotropin-releasing factor inhibits maternal aggression in mice. Behavioral Neuroscience, 118:805-814.

Espana RA, Berridge CW, Gammie SC (2004). Diurnal levels of Fos immunoreactivity are elevated within hypocretin neurons in lactating mice. Peptides, 25:1927-1934.

Gammie SC, Hasen NS, Rhodes JS, Girard I, Garland T (2003). Predatory aggression, but not maternal or intermale aggression, is associated with high voluntary wheel-running behavior in mice. Hormones and Behavior, 44:209-221.

Rhodes JS, Garland T, Gammie SC (2003). Patterns of brain activity associated with variation in voluntary wheel-running behavior. Behavioral Neuroscience, 117:1243-1256.

Lonstein JS, Gammie SC (2002). Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neuroscience and Biobehavioral Reviews, 26:869-888.

Gammie SC, Nelson RJ (2001). cFOS and pCREB activation and maternal aggression in mice. Brain Research, 898:232-241.

Gammie SC, Nelson RJ (2000). Maternal and mating-induced aggression is associated with an elevation of citrulline immunoreactivity in the paraventricular nucleus in prairie voles. Journal of Comparative Neurology, 418:182-192.

Gammie SC, Huang PL, Nelson RJ (2000). Maternal aggression in endothelial nitric oxide synthase-deficient mice. Hormones and Behavior, 38:13-20.

Gammie SC, Olaghere-da Silva UB, Nelson RJ (2000). 3-Bromo-7-nitroindazole, a neuronal nitric oxide synthase inhibitor, impairs maternal aggression and citrulline immunoreactivity in prairie voles. Brain Research, 870:80-86.

Gammie SC, Dawson VL, Nelson RJ (2000). Influence of nitric oxide on neuroendocrine function and behavior. In Nitric Oxide. L. J. Ignarro (editor), pp 429-438. San Diego, Academic Press.

Gammie SC, Nelson RJ (1999). Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. Journal of Neuroscience, 19:8027-8035. (open access)

Demas GE, Kriegsfeld LJ, Blackshaw S, Huang PL, Gammie SC, Nelson RJ, Snyder SH (1999). Elimination of aggressive behavior in male mice lacking endothelial nitric oxide synthase. Journal of Neuroscience, 19:RC30 (open access)

Gammie SC, Truman JW (1999). Eclosion hormone provides a link between ecdysis triggering hormone and crustacean cardioactive peptide in the neuroendocrine cascade that controls ecdysis behaviour. Journal of Experimental Biology, 202:343-352. (open access)

Gammie SC, Truman JW (1997). Neuropeptide hierarchies and the activation of sequential motor behaviors in the hawkmoth, Manduca sexta. Journal of Neuroscience, 17:4389-4397. (open access)

Gammie SC, Truman JW (1997). An endogenous elevation of cGMP increases the excitability of identified insect neurosecretory cells. Journal of Comparative Physiology A, 180:329-338.

Ewer J, Gammie SC, Truman JW (1997). Control of insect ecdysis by a positive-feedback endocrine system: roles of eclosion hormone and ecdysis triggering hormone. Journal of Experimental Biology, 200:869-881. (open access)