Photoperiodic Regulation of Behavioral Responses to Bacterial and Viral Mimetics: A Test of the Winter Immunoenhancement Hypothesis

Abstract

Siberian hamsters (Phodopus sungorus) exhibit changes in immune function following adaptation to short photoperiods, including a marked attenuation of energetically expensive thermoregulatory and behavioral responses to gram-negative bacterial infections. Whether this seasonal attenuation of the immune response is idiosyncratic to gram-negative infections or is representative of innate immune responses in general is not known. If seasonal attenuation of responsiveness to infection is indeed driven primarily by anticipation of energetic constraints, then one would predict that responsiveness to all pathogens would be diminished during short days. If, on the other hand, seasonal changes in responsiveness to infection reflect anticipation of specific pathogens that are common at different phases of the annual cycle, then one would expect short photoperiods to attenuate responsiveness to some pathogens and long photoperiods to attenuate responsiveness to others. To resolve this issue, we exposed male Siberian hamsters to either long or short photoperiods for 11 weeks, then examined their behavioral sickness responses to compounds that represent the minimally immunogenic components of gram-negative bacterial (lipopolysaccharide), gram-positive bacterial (muramyl dipeptide), and viral (polyinosinepolycytidylic acid) organisms. Hamsters exhibited anorexic, anhedonic, ponderal, and/or thermoregulatory sickness behaviors to all 3 pathogen mimetics, but in all cases in which sickness responses were evident, they were attenuated in short days. Energetically costly behavioral responses to several distinct classes of infectious organisms are attenuated in anticipation of winter. The data are not consistent with a pathogen-specific seasonal modulation of innate immune responses.

Seasonal Variation

“…Alternatively, it is certainly possible that the increased mortality in the winter in patients with PF is entirely unrelated to infection and is due to other unidentified seasonalrelated changes (such as in behavioral patterns or environmental alterations), 27,28 or to noninfectious aberrations in immune or mesenchymal cell function induced by other unknown factors. 20,29,30 Similar to other pulmonary conditions in which seasonal variation has been reported and has led to alternative hypotheses, 38 identification of novel risk factors, 39 insight into the mechanisms involved in the pathogenesis of disease, 40,41 and recommendations for changes in health policy, 42 we believe our findings are relevant to better understanding this complex disease. While our study only provides a signal, the identification of seasonal variation in mortality rates from PF has important implications, including improved knowledge of disease epidemiology, an explanation for variability in case-fatality rates between studies 13 and, we believe, insight into the pathogenesis of the ultimate cause of death in these patients.…”

Leptin mediates seasonal variation in some but not all symptoms of sickness in Siberian hamsters

“…To assess the effects of our treatments on hedonic behavior, we provided hamsters with a highly palatable sodium saccharin solution (Baillie and Prendergast, 2008). Beginning 5 days before LPS and saline injections, for the first 6 h of the dark phase (long days: 2000 h to 200 h; short days: 1600 h to 2200 h) hamsters were provided with a fluid bottle containing a solution of 0.1% sodium saccharin (saccharin sodium salt hydrate, Sigma-Aldrich, St. Louis, MO, USA) dissolved in tap water (Baillie and Prendergast, 2008).…”

Immune–neural connections: how the immune system’s response to infectious agents influences behavior

“…The increased resting and diminished grooming are considered sickness behaviors. Interestingly, one of only a handful of studies that compare the behavioral effects of various TLR ligands was performed with MDP, LPS and poly I:C (Baillie and Prendergast, 2008). In this study, i.p.…”