J Comp Physiol A (2005) 191: 231–239 DOI 10.1007/s00359-004-0585-5 REVIEW Robert Huber Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena Received: 2 March 2004 / Revised: 15 October 2004 / Accepted: 30 October 2004 / Published online: 1 February 2005 Ó Springer-Verlag 2005 Abstract Recent investigations in invertebrate neurobi- Introduction ology have opened up new lines of research into the basic roles of behavioral, neurochemical, and physio- ‘‘Under carefully controlled experimental circumstances, logical effects in complex behavioral phenomena, such an animal will behave as it damned well pleases’’—E. O. as aggression and drug-sensitive reward. This review Wilson’s Basic Law of Animal Behavior effectively sums summarizes a body of quantitative work, which identi- up our combined sense of wonder and frustration as fies biogenic amines as a pharmacological substrate for multiple presentations of a specific stimulus rarely evoke motivated behaviors in the crayfish, Orconectes rusticus. identical responses, even under rigorously specified Specifically, this paper details progress that has (1) environmental conditions. Thus, altered responses must explored links between serotonin and an individual’s be attributed to changes in the internal state of an aggressive state, and (2) demonstrated the existence of individual. Terms such as ‘‘specific arousal’’, ‘‘motiva- crayfish reward systems that are sensitive to human tion’’, or ‘‘behavioral state’’ collectively refer to the drugs of abuse, such as psychostimulants. First, we subset of reversible, short-term alterations in behavior summarize a set of experimental approaches that explore that are not associated with fatigue or learning aggression in crayfish and the significance of aminergic (Immelmann and Beer 1989). Used purely as an inter- systems in its control. Agonistic behavior in crustaceans vening concept and without regard to its neural under- can be characterized within a quantitative framework; pinnings, the predictive value of a ‘‘motivation’’ depends different types of behavioral plasticity in aggressive on whether it provides a simpler representation of rela- behavior are in need of physiological explanation, and tionships within the given system (Hinde 1982). It is of pharmacological intervention involving serotonergic little use when we are forced to postulate a separate systems bring about characteristic changes in behavior. motivation for each pattern we wish to explain. Indeed, A second set of experiments demonstrates that psycho- with a full understanding of a particular behavior’s stimulants (cocaine and D-amphetamine) serve as re- causes, we would have no need for such a term at all wards when an intra-circulatory infusion is coupled to a (Dawkins 1995). distinct visual environment. Work in novel model sys- Traditionally, motivations were viewed as individual, tems such as crayfish constitutes a useful comparative unitary properties corresponding to broad behavioral approach to the study of aggression and drug addiction. categories such as eating, parental care, or fighting (Tinbergen 1951). These forces were thought to interact, Keywords Biogenic amine Æ Aggression Æ Agonistic and thereby guide behavior, in a ‘‘great parliament of behavior Æ Motivation Æ Addiction instincts’’ (Lorenz 1966). This classical ethological view of the term ‘‘motivation’’ has not been without its critics, and such models have now largely been superseded by a more complex, multidimensional view, where each par- R. Huber ticular behavioral response arises from the close inter- Center for Neuroscience, Mind and Behavior, action of several independent physiological or stimulus Department of Biological Sciences, axes. In the present paper, we view behavior as a set of Bowling Green State University, individual decisions—each with a particular probability Bowling Green, OH 43403, USA E-mail: [email protected] of occurrence, a motivational context, and controlled by Tel.: +1-419-3727492 the interplay of distinct underlying causative mecha- Fax: +1-419-3722024 nisms. Motivational states thus simply refer to intrinsic 232 forces that promote the occurrence of defined sets of has become increasingly clear that neither the classical behaviors within an adaptive context, without implying ethological nor a traditional neuropharmacological ap- a specific underlying framework (e.g., psycho-hydraulic proach will suffice alone. For an integrated analysis of model—Lorenz 1966, neuro-evolutionary con- neuromodulators in complex behavior, it is essential that structs—MacLean 1990; Panksepp 1998). It is important we combine studies of physiology, biochemistry, phar- to note that without knowledge of their underlying macology, and molecular genetics with quantitative substrates, action tendencies cannot be measured di- behavioral analyses (Lederhendler and Shulkin 2000; rectly but can only be assessed a posteriori through Chen et al. 2002; van Staaden and Huber 2001). observations of behavior under defined circumstances of Aminergic mechanisms that generalize across broad stimulus (Seitz 1940). In some instances, however, esti- taxonomic boundaries reflect an ancient evolutionary mates of behavioral states may be gained via known emergence of amine-signaling mechanisms predating correlates, such as color patterns (Summers and that of the chordate lineage. Specifically, such systems Greenberg 1994; Belthoff and Gowaty 1996; O’Connor share significant commonalities in their neurobiological et al. 1999), social status (Raab et al. 1986; Saltzman substrates: sequence homologies of key receptor ele- et al. 1996; Yang et al. 2001), territoriality (Wazlavek ments (Hen 1992, 1993), pharmacological properties and Figler 1989; Bolyard and Rowland 2000; Ratti (Tierney 2001), methods of inactivation (Porzgen et al. 2000), or neurochemical measures (Yodyingyuad et al. 2001), general modes of action (Vernier et al. 1995, 1985; Dillon et al. 1992; Lopez et al. 2002). 1997), and association with similar behavioral contexts A comprehensive understanding of the causation of (Kravitz 1988, 2000). G protein-coupled, metabotropic behavior, beyond the intervening level of motivations, monoamine receptors appear to have arisen during the requires that behavioral variability is ultimately mapped evolutionary transition to multicellular life (Vernier onto its underlying proximate mechanisms. Monoamine et al. 1995). Presumably, early metazoans adopted systems are attractive candidates for the control of such monoamine systems to represent global motivational motivational axes as they modify neural function at states, which coordinate functions of individual cells in multiple levels and may thereby bring about coordinated different parts of the body for adaptive responses to- responses to environmental perturbations (Libersat and wards environmental perturbations. Due to phyloge- Pflu¨ ger 2004). Neuromodulators and neurohormones netic conservation, vertebrates and invertebrates offer are generally considered to selectively sensitize or de- significant homologies within functional sets of receptor press sensory elements, organize neuronal activity in families (Peroutka and Howell 1994; Walker et al. 1996; central circuits, or bias motor systems towards contex- Chan and Jan 1999). Since the Precambrian, however, tually appropriate states (e.g., Harris-Warrick and independent evolutionary paths have given rise to the Kravitz 1984; Beltz and Kravitz 1986; Beyer and Feder present-day diversity of (ortho as well as paralogous) 1987; Bicker and Menzel 1989). In this manner, amines subtypes, their respective pharmacological profiles, and are thought to alter the activity of specific neural deci- individual links with specific behaviors. sion-making centers (Nader et al. 1997). Rather than Crayfish have continued to play a unique role among produce behavior per se, these substances appear to tune invertebrate models for studies of mechanisms due to a ongoing activity and, in a given context, promote the nervous system that is uniquely accessible to a wide occurrence of adaptive behaviors (e.g. feeding, flight, range of behavioral, neural, and neurochemical ap- fight, or mating) over contraadaptive ones (Kravitz proaches. Behaviors contain stereotyped elements and 1988; Libersat and Pflu¨ ger 2004). Considerations about its CNS consists of relatively few, large, recognizable their specificity reflect shifts in our expectations from a neurons embedded within a well-characterized func- view of neural mechanisms ‘‘for’’ a particular behavior, tional neuroanatomy for modulatory substances (Kra- to one that modifies neural environments ‘‘fostering’’ the vitz 1988, 2000; Libersat and Pflu¨ ger 2004). Offering occurrence of specific behaviors (Heinrich et al. 2001; greatly reduced complexity compared to any other ver- van Staaden and Huber 2001). Such systems are par- tebrate, its main strength lies in experimental opportu- ticularly difficult to study in behavioral contexts since nities to first identify and then obtain a detailed aminergic neurons send extensive projections across understanding of the inner workings at key neuronal large areas of nervous tissue (Azmitia and Segal 1978; sites for the behavioral plasticity in question. However, a Lidov and Molliver 1982; Beltz and Kravitz 1987)to comprehensive framework linking neuromodulator respective targets that possess a full complement of function with motivated behavior has remained elusive. receptors, each with a unique coupling mechanism and Recent work has helped to extend