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Functional Mapping of the Prosencephalic Systems Involved in Organizing Predatory Behavior in Rats

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Functional Mapping of the Prosencephalic Systems Involved in Organizing Predatory Behavior in Rats Neuroscience 130 (2005) 1055–1067 FUNCTIONAL MAPPING OF THE PROSENCEPHALIC SYSTEMS INVOLVED IN ORGANIZING PREDATORY BEHAVIOR IN RATS E. COMOLI,a É. R. RIBEIRO-BARBOSA,a N. NEGRÃO,a Predatory hunting has been regarded as an innate behav- M. GOTOb AND N. S. CANTERASa* ioral response seemingly critical for the animals’ survival aDepartment of Physiology and Biophysics, Institute of Biomedical (Eisenberg and Leyhausen, 1972). Most of our knowledge Sciences, University of São Paulo, Avenida Lineu Prestes, 1524, CEP regarding the neural basis of this behavior derives from 05508-900 São Paulo, SP, Brazil studies done in the 1960s and 1970s, based on the use of bNeuroscience Laboratory II, City University of São Paulo, Rua lesion and electrical stimulation methods in cats and ro- Cesário Galeno, 475, CEP 00307-000 São Paulo, SP, Brazil dents. These studies suggest that the organization of pred- atory attack depends upon sites along the length of the Abstract—The study of the neural basis of predatory be- lateral hypothalamus and is mediated by a descending havior has been largely neglected over the recent years. limb of the medial forebrain bundle passing through the Using an ethologically based approach, we presently de- ventral tegmental area to the ventral mesencephalic and lineate the prosencephalic systems mobilized during pre- pontine tegmentum (Egger and Flynn, 1963; Sheard and dation by examining Fos immunoreactivity in rats perform- Flynn, 1967; Chi and Flynn, 1971; Bandler et al., 1972; ing insect hunting. These results were further compared Berntson, 1972, 1973; Proshansky et al., 1974). with those obtained from animals killed after the early However, due to methodological constraints, these nocturnal surge of food ingestion. First, predatory behav- studies were limited in terms of providing a clear definition ior was associated with a distinct Fos up-regulation in the of the neural systems underlying predatory behavior that ventrolateral caudoputamen at intermediate rostro-caudal levels, suggesting a possible candidate to organize the occurs under natural conditions. This seems to be partic- stereotyped sequence of actions seen during insect hunt- ularly true for the studies on rodents, where, depending on ing. Insect predation also presented conspicuous mobili- the intensity of stimulation, a variety of aggressive re- zation of a neural network formed by a distinct amygdalar sponses—ranging from defensive to quiet biting attack— circuit (i.e. the postpiriform-transition area, the anterior could be evoked from what had been defined as the hy- part of cortical nucleus, anterior part of basomedial nu- pothalamic attack area (see Siegel et al., 1999). cleus, posterior part of basolateral nucleus, and medial An ethologically based approach for studying preda- part of central nucleus) and affiliated sites in the bed nuclei tory behavior was attempted with the mouse-killing para- of the stria terminalis (i.e. the rhomboid nucleus) and in the digm, largely explored by Karli and colleagues (Vergnes hypothalamus (i.e. the parasubthalamic nucleus). Accord- ingly, this network is likely to encode prey-related motiva- and Karli, 1963, 1972; Chaurand et al., 1972; Vergnes, tional values, such as prey’s odor and taste, and to influ- 1975). Unfortunately, this paradigm presents serious limi- ence autonomic and motor control accompanying preda- tations constraining its use. Animals need to be food de- tory eating. Notably, regular food intake was also prived for a few days to present mouse-killing behavior, associated with a relatively weak Fos up-regulation in this which will be expressed only by a small percentage of rats network. However, during regular surge of food intake, we (around 16%; Vergnes, 1975). Moreover, the confrontation observed a much larger mobilization in hypothalamic sites with a live mouse is frequently associated with overt de- related to the homeostatic control of eating, namely, the fensive reactions, such as freezing and flight; therefore, arcuate nucleus and autonomic parts of the paraventricu- part of the attack episodes may be, in fact, related to lar nucleus. Overall, the present findings suggest potential neural systems involved in integrating prey-related moti- defensive behavior. vational values and in organizing the stereotyped se- To circumvent these problems, insect hunting appears quences of action seen during predation. Moreover, the as an ideal condition to investigate predatory behavior in comparison with regular food intake contrasts putative rats. In this paradigm, roaches have been chosen as suit- neural mechanisms controlling predatory related eating vs. able prey, since they are relatively innocuous and easily regular food intake. © 2005 Published by Elsevier Ltd on overcome; likewise, they do not seem to induce apprecia- behalf of IBRO. ble defensive reactions in rats. In addition, considering the voracity that the rats present to consume the roaches, they Key words: aggression, feeding behavior, amygdala, hypo- thalamus, basal ganglia. are supposedly very palatable with potentially high hedonic value. Remarkably, in a recent work, we were able to *Corresponding author. Tel: ϩ55-11-3091-7628; fax: ϩ55-11-3091- demonstrate that insect predation and exposure to a nat- 7285. ural predator induce an opposite activation pattern of the E-mail address: newton@fisio.icb.usp.br (N. S. Canteras). periaqueductal gray, reflecting, perhaps, the diverse moti- Abbreviations: ABC, avidin–biotin complex; BST, bed nuclei of the stria terminalis; Fos-ir, Fos immunoreactive; fx, fornix; GPl, globus vational drives underlying each of these responses pallidus, lateral segment; MCH, melanin-concentrating hormone. (Comoli et al., 2003). Importantly, as confirmed for several 0306-4522/05$30.00ϩ0.00 © 2005 Published by Elsevier Ltd on behalf of IBRO. doi:10.1016/j.neuroscience.2004.10.020 1055 1056 E. Comoli et al. / Neuroscience 130 (2005) 1055–1067 different rat strains tested, cockroach predation has been was always stained with Thionin to serve as a reference series for shown to be vividly expressed by all individuals (Rebouças cytoarchitectonic purposes. and Schmidek, 1997). The relative strength of expression of Fos immunoreactivity was evaluated by an observer without the knowledge of the ex- In the present study, we attempted to delineate the perimental status using a semiquantitative rating scale derived prosencephalic sites involved in the integration of innate from the mean values of Fos labeling density. In all animals of predatory responses by examining Fos immunoreactivity each experimental group, these measurements were taken from in the prosencephalon of rats performing insect hunting. To the prosencephalic regions, which were individually outlined at a differentiate the Fos increase likely to be related to food selected level, and the Fos-labeled cells and the outlined area intake, the results were further compared with those ob- were quantified using a Nikon Eclipse E600 microscope (Nikon, ϫ tained from animals killed after the early nocturnal surge of Japan) (10 magnification) equipped with a Spot digital camera (Diagnostic Instruments, Inc., Sterling Heights, MI, USA) inter- food ingestion. faced to an image analysis system (Image-Pro Plus; Media Cy- bernetics, Silver Spring, MD, USA). EXPERIMENTAL PROCEDURES To provide an independent assessment of the validity of these ratings, counts of the number of Fos immunoreactive (Fos-ir) neu- Adult male Wistar rats (nϭ15), weighing about 250 g and obtained rons as a function of experimental status were generated for selected from the local breeding facilities, were used in the present study. cell groups by using the 10ϫ objective of a Nikon Eclipse E600 The animals were kept under controlled temperature (23 °C) and microscope equipped with a camera lucida. These were performed illumination (12-h light/dark cycle) in the animal quarters, and had by counting all Fos-ir nuclei in a complete series of sections (where free access to water and standard laboratory diet (Nutrilab CR1; the sections were 120 ␮m apart) through the structures of interest, as Nuvital Nutrientes, Ribeirão Preto, SP, Brazil). Experiments were defined in adjoining Thionin-stained series. The extrapolating esti- carried out in accordance with the National Institutes of Health mated counts were obtained by using the method of Abercrombie Guide for the Care and Use of Laboratory Animals (1996) and the (1946) that takes into account the crude count of number of Fos-ir University of São Paulo’s Institute of Biomedical Sciences Com- nuclei seen in the sections, the thickness of the sections and the mittee for Ethics and Animal Care in Experimental Research. In average length of the Fos-ir nuclei. These data were analyzed by a the present study, we attempted to minimize the number of ani- multivariate analysis of variance (one way MANOVA, where we mals used and their suffering. treated cell counting in each selected region as dependent variables, One week before the experimental procedures, animals were and the experimental groups as the between-group independent individually housed into a Plexiglas cage (50ϫ35ϫ16 cm), and variable), followed by multiple comparisons using the Tukey HSD were handled repeatedly by the same investigator who conducted test. The significant level was set at 5%. All the values are expressed the behavioral tests. Two experimental groups were tested be- as meanϮS.E.M. tween 15:00 and 16:00 h. One of these group of animals (nϭ5) The figures were prepared for publication by using
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