Ph.D., Cornell University, 1998 Assistant Professor Member, Neuropsychology and Behavioral Neuroscience Program (NBN) apetrulis@gsu.edu 404-413-6290 219 Kell Hall

Research Program

My general interest is in understanding how the nervous system processes and integrates social information and how this information is then used to adaptively regulate social behavior. I am also interested in studying how gonadal steroid hormones alter neural processing of social cues. In particular, my work is focused on analyzing the neurobiology of odor or "pheromonal" communication in Golden hamsters, a species that relies heavily on scent to guide its social behavior. This laboratory uses a variety of techniques, including detailed behavioral analysis, permanent and reversible brain lesions, manipulations of endocrine systems, intracranial delivery of drugs and sex steroids, immunocytochemical detection of cellular activation and electrophysiological recordings from single neurons in awake and behaving animals to answer two specific questions:

How does the brain recognize the sex of other animals and how does that lead, in turn, to sexual attraction? Previous work has demonstrated that an interconnected set of brain structures, sensitive to sex steroids, is critical for many social behaviors such as copulation, aggressive and maternal behavior. Evidence has accumulated that some of these same structures in the amygdala and hypothalamus may also be involved in attraction to, and preference for, opposite-sex conspecifics. I have identified circuits in the hamster brain that are involved in regulating preferences to approach and investigate opposite-sex odors as well as regulating scent-marking responses to these odors (Petrulis & Johnston, 1999; Petrulis, Peng & Johnston 1999a,b). As sociosexual interest toward potential mates involves a complex interplay between internal state variables, such as gonadal steroid levels, and external cues, such as species-specific odors, my current focus is aimed at understanding how the neural integration of hormonal and social cues generates sexual attraction and preference in male hamsters. Although we do not know where this interaction occurs to regulate sexual attraction, there is evidence suggesting that this might occur within two forebrain areas, the medial amygdala (MA) and bed nucleus of the stria terminalis (BNST). The MA and BNST are divided into two separate and parallel circuits, one receiving primarily chemosensory input and the other having extensive steroid receptor distribution.

One way in which steroids and female chemosignals could interact is that the chemosensory sub-regions of MA/BNST provide non-specific modulatory input to the steroid-sensitive sub-regions, which in turn, act to discriminate between social odors. We have termed this the gate hypothesis. In contrast, another hypothesis, which we have termed the modulation hypothesis, suggests that the chemosensory MA/BNST mediates the fast-acting, evaluative processes underlying recognition of male and female odors, while the steroid-sensitive regions of BNST and MA mediate the slow-acting, non-specific modulatory effects on processing in chemosensory areas.

We are testing between the modulation and gate hypotheses using two strategies. First, we are using lesions to dissociate the functions of chemosensory and steroid-sensitive regions of MA and BNST. Second, we are, for the first time, defining the representation of sexual odors in MA and BNST by combining behavior with single-neuron and population electrophysiological recording in awake, behaving animals.

How does the brain learn and remember social information? Animals often learn associations between social odor cues and particular social outcomes that they can then use to alter their future social behavior. For example, we have demonstrated that hamsters react with greater fear/anxiety when exposed to animals that defeated them in an aggressive encounter than to other unfamiliar, dominant animals (Petrulis, et al, 2004). Moreover, male hamsters show olfactory preferences for novel females rather than for females with whom they have already mated (Petrulis & Eichenbaum, 2003b). Both of these results indicate that hamsters are able to remember odors associated with familiar animals and to act accordingly. Although the neural circuits underlying social odor memory are not well defined (Petrulis & Eichenbaum, 2003a), I have identified one crucial structure of this circuit, the entorhinal cortex surrounding the hippocampus, that is involved in discrimination and recognition of familiar individuals from unfamiliar conspecifics (Petrulis, Peng & Johnston, 2000). Moreover, neurons in the entorhinal cortex respond to changes in the familiarity of individual's odors (Petrulis, Alvarez & Eichenbaum,2005). My aim is to further define the circuitry underlying the acquisition, consolidation and expression of social odor memory in the context of aggressive and sexual behavior.

Representative Publications

Currently Funded Federal Grants

Principal Investigator, “Neurobiology of Social Attraction and Preference” NIMH (RO1MH072930-01), 2005-2010, $950,000 (direct costs).

Principle Investigator, “The function of c-fos in sexual behavior” National Science Foundation, Science and Technology Center Venture Grant, 2003-2005, $30,000 (direct costs).

Representative Publications

Petrulis, A. & Johnston, R. E. (1995) A re-evaluation of dimethyl disulfide as a sex attractant in golden hamsters. Physiology and Behavior, 57, 779-784.

Petrulis, A. & Johnston, R. E. (1995) Odor modulation of scent marking in female golden hamsters. In R. Apfelbach, D. Muller-Schwarze, K. Reutter & E. Weiler (Eds.), Advances in Biosciences: Vol. 93. Chemical Signals in Vertebrates 7 (pp. 353-360). Oxford: Pergamon Press.

Petrulis, A. & Johnston, R. E. (1997) Causes of scent marking in female golden hamsters (Mesocricetus auratus): specific signals or classes of information? Journal of Comparative Psychology, 111, 25-36.

Petrulis, A., deSouza, I., Schiller, M. & Johnston, R. E. (1998) Role of frontal cortex in social odor discrimination and scent-marking in female golden hamsters (Mesocricetus auratus). Behavioral Neuroscience, 112, 199-212.

Petrulis, A. & Johnston, R. E. (1999) Lesions centered on the medial amygdala impair scent-marking and sex odor recognition but spare discrimination of individual odors in female golden hamsters (Mesocricetus auratus). Behavioral Neuroscience,113, 345-357.

Petrulis, A., Peng, M. & Johnston, R. E. (1999a) Lateral olfactory tract transections impair discrimination of individual odors, sex odor preferences and scent-marking in female golden hamsters (Mesocricetus auratus). In R. E. Johnston, D. Muller-Schwarze & P. Sorensen (Eds.), Advances in Chemical Communication in Vertebrates (pp. 549-562). New York: Plenum Press.

Petrulis, A., Peng, M. & Johnston, R. E. (1999b) Effects of vomeronasal organ removal on individual odor discrimination, sex odor preference and scent marking by female golden hamsters (Mesocricetus auratus). Physiology and Behavior, 66, 73-83.

Petrulis, A., Peng, M. & Johnston, R. E. (2000) The role of the hippocampal system in social odor recognition and scent marking by female golden hamsters (Mesocricetus auratus). Behavioral Neuroscience, 114, 184-195.

Petrulis, A. & Eichenbaum, H. (2003a) Olfactory memory. In R. L. Doty (Ed.), Handbook of Olfaction and Gustation: Second Edition. New York: Marcel Dekker, 409-438.

Petrulis, A. & Eichenbaum, H. (2003b) The perirhinal-entorhinal cortex, but not the hippocampus, is critical for expression of individual recognition in the context of the Coolidge effect. Neuroscience, 122, 599-607.

Petrulis, A., Weidner, M. & Johnston, R. E. (2004) Recognition of competitors by male golden hamsters. Physiology and Behavior, 81, 629-638.

Petrulis, A., Alvarez, P. & Eichenbaum, H. (2005) Neural correlates of social odor recognition and the representation of individual-distinctive social odors within entorhinal cortex and ventral subiculum. Neuroscience, 130, 259-274.

Petrulis, A. (2005) The neurobiology of odor-based sexual preference: the case of the Golden hamster. In R. T. Mason, M. P. LeMaster & D. Muller-Schwarze (Eds.), Chemical Signals in Vertebrates 10 (pp. 291-299). New York: Springer.

Maras, P. & Petrulis, A. (2006) Chemosensory and steroid-responsive regions of the medial amygdala regulate distinct aspects of opposite-sex odor preference in male Syrian hamsters. European Journal of Neuroscience, 24, 3541-3552.

Eidson, L., Maras, P., Epperson, E. & Petrulis, A. (2007) Female hamster preference for odors is not regulated by circulating gonadal hormones. Physiology and Behavior, 91, 134-141.

Maras, P. & Petrulis, A. (2007) The role of early olfactory experience in the development of adult odor preferences in rodents. In J. Hurst, R.J. Beynon, S.C. Roberts & T. Wyatt (Eds.), Chemical Signals in Vertebrates 11, (pp. 251-260). New York: Springer.

Been, L. & Petrulis, A. (2007) The neurobiology of sexual solicitation: vaginal marking in female Syrian hamsters (Mesocricetus auratus). In J. Hurst, R.J. Beynon, S.C. Roberts & T. Wyatt (Eds.), Chemical Signals in Vertebrates 11, (pp. 231-239). New York: Springer.