Stability and flexibility of the message carried by semiochemical stimuli, as revealed by devaluation of carbon disulfide followed by social transmission of food preference

Autor: Donald B. Katz, Nicholas C. Barry, Joost X. Maier, Meredith L. Blankenship, Sarah E. Richards
Rok vydání: 2014
Předmět:
Zdroj: Behavioral Neuroscience. 128:413-418
ISSN: 1939-0084
0735-7044
Popis: Animals communicate with each other using a wide variety of physical and chemical signals. The meaning of such signals—their significance to the conspecific being communicated with—is often flexible, and can be influenced by experience, a prime example being the malleability of human language. The meaning of semiochemicals (the class of chemical signals that includes pheromones), on the other hand, is thought to be highly stable. Semiochemicals, by definition, are organism-emitted cues that carry intrinsic value and elicit specific behavioral or physiological responses that are mediated by highly sensitive and highly specific olfactory pathways in the main and accessory olfactory systems (Hu et al., 2007; Leinders-Zufall et al., 2007; Leinders-Zufall et al., 2000; Liberles & Buck, 2006). Recent work demonstrates, however, that semiochemicals also activate canonical olfactory pathways—that is, G protein-coupled olfactory sensory neurons (OSNs) in the main olfactory epithelium that are responsible for odor perception (D. Y. Lin, Zhang, Block, & Katz, 2005; W. Lin, Arellano, Slotnick, & Restrepo, 2004; Luo, Fee, & Katz, 2003; Munger et al., 2010; Xu et al., 2005). This fact suggests that semiochemical perception may be subject to experience-dependent plasticity typically associated with processing in the canonical olfactory pathway (Mandairon & Linster, 2009). The degree to which the multiple pathways activated by the same semiochemical interact, and what the behavioral consequences of such interactions are, remains a topic of debate (Munger, Leinders-Zufall, & Zufall, 2009). For instance, can an intrinsically positive semiochemical be rendered aversive, and if so, does this learned aversion impede its semiochemical function? In the present work, we assessed the independence of rats’ canonical (olfactory) and semiochemical perception of carbon disulfide (CS2)—a semiochemical that communicates consumability of a food from one conspecific to another (B. Galef, Mason, Preti, & Bean, 1988; Munger et al., 2010). CS2 is a dominant and highly volatile component of rodent breath that, when smelled in combination with a food odor, increases preference of the observer for that food (Fortis-Santiago, Rodwin, Neseliler, Piette, & Katz, 2010; B. Galef et al., 1988; B. G. Galef & Wigmore, 1983; Munger et al., 2010). CS2-mediated social transmission of food preference from demonstrator to observer can occur with exposure as brief as 5 minutes (Burne, Johnston, Wilkinson, & Kendrick, 2010) and is highly robust. For example, preferences are effectively transmitted even when the food is aversive (B. Galef et al., 1988), and even when the demonstrator is prone, ill, or unconscious (Burne et al., 2010; B. G. Galef, Jr., Wigmore, & Kennett, 1983). Thus, preference induction by CS2 apparently involves little evaluation of current context, suggesting that the meaning of CS2 may be independent of experience—i.e., stable and unmodifiable. This semiochemical function of CS2 appears to begin with transduction via a specialized subset of OSNs expressing guanylyl cyclase D (GC-D) receptors. However, CS2 also appears to activate canonical OSNs in addition to GC-D OSNs (Munger et al., 2010). In order to test the hypothesis that CS2 is processed by two separate neural pathways, we first attempted to condition an aversion to CS2, using a taste-potentiated odor aversion paradigm; subsequently, we tested the same animals’ ability to use CS2 as a semiochemical in learning socially transmitted food preferences. The results demonstrate that rats indeed learn aversions to CS2, just as they learn aversions to commonly used non-pheromonal odors. CS2-induced food preference learning, however, is unimpeded by this newfound aversion. These data imply the existence of multiple independent olfactory processing systems, supported either by multiple transduction pathways or contextual variables that emphasize activity in one activated circuit over another.
Databáze: OpenAIRE