Insights from rodent food protection behaviors

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Insights from rodent food protection behaviors Megan Marie Martin St. Peters ∗ Ferrum College, P.O. Box 1000, Ferrum, VA 24088, United States

a r t i c l e

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Article history: Received 1 October 2016 Received in revised form 9 January 2017 Accepted 9 January 2017 Available online xxx Keywords: Rat Food protection Natural defensive behavior Ethology Dodging

a b s t r a c t This review aims to provide an update on the current state of research in food protection behaviors. This includes a detailed description of food protection behaviors, theoretical considerations, neuroscientific results, a separate examination of robbers’ behaviors, and some suggestions on future studies. The goal is to provide a succinct overview of food protection behaviors while showcasing their usefulness through an ethologically gestalt lens in which to examine underlying systems of interest not only to better understand the species, but also as an antecedent for understanding human behaviors and conditions. © 2017 Elsevier Inc. All rights reserved.

1. Introduction Food protection behaviors have been used to explore cognitive and motor behaviors in rats from developmental, neurological, and social perspectives for nearly 30 years. This laboratory paradigm has been developed by Whishaw and Tomie originally for use as an ethological tool for investigating sensorimotor problems (Whishaw & Tomie, 1988). It has since revealed insights into development of sex differences in food protection behaviors, roles of hormones, sensory systems, neural systems, and cortical regions. Food protection behaviors have been discussed in terms of motor action patterns, interval timing theory, and mobility gradient theory. Although ethological researchers appreciate the diverse interpretations enabled by the study of natural behaviors, one of the goals of this review is to showcase the usefulness of food protection behaviors not only from an ethological lens, but also as a means to better understand human behaviors and conditions. Recent neuroscience research with rats typically aim to model human clinical or neurological disorders by means of designs that enable precision and control (e.g., operant boxes, water maze). Natural behaviors however have their own merits, a large one being they do not require training or shaping. Psychology as a discipline has a torrid history of being “all or none”. For instance, the years of debates on nature versus nurture. Now most psychologists appreciate that nurture works through what nature endows. Similarly, precision and control offer great starting points for understanding constructs but ecological approaches may provide unique insights into how animals function in more realistic situations. This review aims to offer more than a plea for these two perspectives to “play nice”. Naturally occurring behaviors, such as food protection behaviors in rodents, occur spontaneously and are multifaceted, providing a rich context for careful analysis that is useful to ethologists as well as applied psychologists. In this article, I review empirical studies examining food protection behaviors, discuss various methods of study, explore interpretations of converging results, and identify areas of future study. Although food protection behavior analyses enables

∗ Corresponding author. E-mail address: [email protected] http://dx.doi.org/10.1016/j.lmot.2017.01.004 0023-9690/© 2017 Elsevier Inc. All rights reserved.

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specific hypotheses concerning individual constructs such as attention, memory, and motivation, it also enables researchers to evaluate whether holistic behavior and its neuroscientific basis is an interaction of many factors which may, in fact, differ than the sum of its parts. 2. Food protection behaviors description Rats are opportunistic feeders, and most food is eaten but can be occasionally carried away. Whether food is eaten or carried away appears to depend on the familiarity and level of threat from conspecifics and/or predators (Whishaw, 1988). Indeed, since rats are opportunistic and eat where food is found, they appear to periodically stop to assess their safety. For instance, on a small stand in an open room, rats pause and use head movements during eating to look around lighted room every 2–3 s, even more often with larger food items. They also eat 20% more quickly in light during than in the dark (Whishaw, Gorny, & Dringenberg, 1991). Data suggests that food protection behaviors are only utilized if the robber is familiar and is deemed non-threatening (Whishaw & Tomie, 1987), which is consistent with expected behavior of territorial animals when confronted with an intruder (Adams, 1976; Blanchard, Blanchard, Takahashi, & Kelley, 1977; Whishaw, Oddie, McNamara, Harris, & Perry, 1990). In contrast, when approached by predators, rats appear more likely to engage in food carrying behavior (Whishaw et al., 1991). Food protection behaviors involve movements that are constant and predictable, suggesting they are unconditioned, species-typical, stereotyped action patterns (Whishaw, 1988; Whishaw & Tomie, 1987). They include clearly identifiable elements such as the head, trunk, and paw movements, kinematic profile, and endpoint (Field, Whishaw, & Pellis, 1996). The vast majority of food protection behaviors have been published involving rat food protection interactions with conspecifics. Food protection behaviors initiate once the approaching rat (“robber”) inserts its snout under the victim and attempts to grasp its food (Whishaw, 1988). Whishaw and Tomie suggest this may be adaptive insofar as the robber is then committed and a dodge will place it inconveniently behind the victim (Whishaw & Tomie, 1987). On over 93% (Whishaw & Tomie, 1987) of robbery attempts, the victim evades the robber using at least two different sequences of movement to protect their food, referred to hereafter as “dodging” and “bracing”. Dodging is when the animal places the food item in its mouth to use all limbs to evade the robber. The movement is typically initiated with the forepaws then the contralateral rear limb, followed by the ipsilateral real limb to evade the robber, before transferring the food back to the forepaws to continue eating, although there are slight variations documented (Whishaw, 1988; Whishaw & Tomie, 1987). Bracing is when the animal continues to grasp the food by the front paws and merely rotates the body from the midsection to the head contralateral to the approach of the robber. Dodging results in a farther displacement. Dodging occurs approximately 78.3% of the time, whereas bracing occurs 21.7% of the time (Whishaw & Tomie, 1987). These behaviors are observed regardless of enclosure, from in housing cages, to small and large experimental enclosures (Whishaw & Tomie, 1987). 2.1. Methodological details Various methods have been used to examine food protection behaviors. Through the testing duration, rats can be doublehoused and maintained on a partial food deprivation schedule, to maintain body weight at approximately 90% of free feeding body weight. Before testing, rats are adapted to the apparatus, testing procedure, and food items to be used during the experiment. Rats are habituated until they continue eating even when another rat is placed in the enclosure. Rats are tested in pairs, with any pairing possibility (testing rats with their housemate e.g., (Whishaw & Gorny, 1994)), use of a dominant robber (Martin et al., 2008), or even a conspecific of the opposite sex (Field, Whishaw, & Pellis, 1997). The apparatus is typically made of a thin Plexiglas cylinder, approximately 40 cm in diameter and 45 cm high (e.g., (Martin et al., 2008; Whishaw & Gorny, 1994)). It is placed on a table with a clear glass top. An inclined mirror, through which the rats can be viewed and videotaped, is located underneath the table to enable the movements of the animals to be measured in two dimensions. See Fig. 1 for an example of the apparatus set-up. A typical testing day consists of placing a rat (the victim) in the cylinder and then placing a food item on the floor in front of the victim so that it only has to walk forward to retrieve it. Once it begins eating, a second rat (the robber) is gently placed, facing the same direction, into the cylinder beside the victim. Thus, the robber need only walk forward to attempt to steal the food. Trials are video-taped until the food item is consumed. If the item is successfully robbed, the food item can be removed from the robber and either returned to the victim (e.g., to examine the time estimations and/or transition from dodging to bracing), or the victim can be given another food item (to maintain dodging vigor, particularly useful in unilateral neglect studies). Kinematic analyses can further document motor abilities by means of average speeds during dodging and bracing behaviors as well as distance traveled by the victim during dodging and bracing. Distance and speed can be more easily quantified by digitizing food protection sequences using a motion measurement system, such as the Peak Performance Technologies, Inc. (Englewood, CO), which permits the digitizing of 60 fields per second. For motion analysis, the center of the food pellet in the mouth, the midbody, and the base of the tail are digitized in the victim (Pellis et al., 1996) or the tip of the snout, a mid-point along the longitudinal axis of the body, and the base of the tail (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997). Depending on the goals of the study, the tip of the snout only is often used to examine robber behaviors, but three or more points can be identified if you are interested in studying the kinematics of the robber as well. See Fig. 2 for Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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Fig. 1. A photograph of the apparatus used in Martin et al., 2008. The apparatus is made of thin plexiglas and a mirror is inclined underneath to permit easy recording of the animals from the ventral perspective.

Fig. 2. Behaviors were recorded from underneath, as shown in a photograph of the apparatus with a victim (blue) and robber (red) present (top left column). The top right column displays the digitization of the rats’ bodies: tip of nose, between the forelimbs, and base of tail at the start of the trial (blue for victim; red for robber). The bottom panel displays the moment-by-moment kinematic profiles of the victim (blue) and robber (red) rats provided by the digitization. The first large blue peak represents a dodge; the second blue peak represents a brace by the victim. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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an example video capture of food protection behaviors with digitized points on the victim and robber, and the kinematic output. 2.2. Variations in experimental design/factors to consider Strain, conspecific familiarity, sex, analysis variations, and hedonic value are variables easily manipulated in the research design when examining food protection behaviors. More research is needed on differences among strains in food protection behaviors. No difference was observed between Long-Evans and Sprague-Dawley rats in display of food protection behaviors (Whishaw, DuBois, & Field, 1998), although kinematic analyses were absent and would be useful. Other strains have yet to be examined but home defense research suggests strains may have different strategies/abilities. For instance, it has been shown that defense of home regions vary widely depending on the strain of rats, with most, such as the DA, Irish, and Lewis strains of rats defending their home region by unfamiliar male conspecifics using full aggressive posture and biting attacks (Adams, 1976) whereas territory-inhabiting albino rats exhibited very low frequency and intensity of agonistic behaviors (Fass, Gutermann, & Stevens, 1979). Also, although isolation-induced fighting involves different stereotyped behaviors heavily influenced by olfaction, it is interesting to note that DA, Irish, Lewis, and Fisher strains all show similar isolation-induced fighting whereas the WAG-Rij rats did not show isolation-induced fighting (Adams, 1976). Olfaction in isolation-induced fighting appears to help trigger offensive or defensive behaviors depending on the interactions between cage odor and other rat familiarity (Adams, 1976). Such interactions may be of interest to explore in food protection behaviors. Home versus intruder rats show differential behaviors when involved in isolation-induced fighting may be of interest to see how animals organize food protection behaviors when the robber is presented first, followed by a victim who is then given a piece of food. Sex of the victim and robber must also be considered. If a novel unfamiliar female robber is introduced, a female victim will drop the food and investigate the robber. If the robber is a male, the female will always drop the food to investigate. If the victim and robber are both male, the victim may piloerect, drop the food, and threaten the robber. If both the victim and robber are older males, they typically fight (Whishaw & Tomie, 1987). There are several variations in analysis one can consider. In some events, it may be of use to manipulate when during the consumption of the food item a robbing attempt occurs, and/or from which side (e.g., in unilateral damage studies). Several publications successfully presented the robber manually so that the time and/or side of approach can be manipulated, as the magnitude and probability of food protection behavior is still modulated by time left to consume the food item (as in Whishaw and Gorny, 1994). Others present new food items when one is stolen to ensure maximum behaviors (thereby exclusively examining dodging, but not bracing behaviors) (e.g., Field et al., 1996; Pellis, Field, & Whishaw, 1999). Rats use temporal information to organize movements in the natural behavior of protecting food from theft by a conspecific robber (Wallace, Wallace, Field, & Whishaw, 2006; Whishaw & Gorny, 1994). Time remaining to consume a food item is the best predictor for the magnitude of food protection behavior associated with food items of varying size. Many food items have been used to examine food protection behaviors, such as precision food pellets ranging in size from 20 to 1000 mg (e.g., Bioserve Inch, Frenchtown NJ), to natural foods such pearl barley, spring wheat, mung beans, azuki bean (Whishaw & Gorny, 1994) and approximate 2.5 g food pellets (Field, Whishaw, Forgie, & Pellis, 2004), almond halves (Himmler et al., 2014), hazelnuts (Martin et al., 2008), and fruit loops (Oddie, Kirk, Gorny, Whishaw, & Bland, 2002). Average eating times of all items reported above were not provided, but the natural grains and nuts take longer to consume yet weigh less than the precision pellets examined by (Pellis et al., 2006; Whishaw & Gorny, 1994), and hazelnuts in the study by Martin and colleagues took longer than any of the eating times reported of the natural grains and nuts used by Whishaw and Gorny (hazelnut took 122.8 s with a SEM 44.2 s – (Martin et al., 2008)). In fact, Whishaw and Gorny (1994) systematically investigated the relationship between food size and hardness with size of food protection behavior and found that in general, longer consumption times were associated with movements that displaced the rat farther away from the conspecific, suggesting that organization of food protection behaviors depend on an animal’s ability to generate an accurate estimate of time left to finish consuming a food item in the seconds-to-minutes range, i.e. interval timing. This is further evidenced by a study showing that if behavior is analyzed for the entire duration of consumption of a single food item, one sees larger displacements of dodging in earlier stages of food consumption and a transition to bracing, which is a much smaller movement in the last portion of food consumption (Martin et al., 2008). Interval timing is discussed in terms of several theories, such as the three stages of information processing as outlined by Meck and colleagues (e.g., (Matell & Meck, 2000)). The clock, memory, and decision stages have been differentiated in behavioral and pharmacological on interval timing in operant procedures (e.g., (Meck, 1996; Wearden, 1999)) as well as the clock stage in food protection behaviors (Martin et al., 2008; Wallace et al., 2006). Although many studies provide new food items to animals to maintain the dodge vigor for kinematic comparisons, it is also insightful to examine the transitions between dodging and bracing throughout the consumption of a single food item. This will be discussed in more detail later. Current interpretations of what motivates a victim to evade its robber involves hedonic value/food hardness. Currently these terms are interchangeable in the literature, but this may be due to the lack of scope of studies examining motivational factors in food protection. Food hardness could also be separated into artificial laboratory precision pellets versus natural foods and grains that animals would find in the wild. If possible, controlling the amount of compression in the laboratory precision pellets so that size is the same but amount of time to eat it varies, would provide more insight into motivational factors. The relationships of caloric intake to “hedonic value” could also be explored. Future studies can examine which drug conditions and/or consumption conditions (i.e. eating alone or with the robber) systematically affect aspects of food Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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protection behaviors that may be impacted by hedonic value (e.g., likelihood of dodging, amount of displacement, speed of displacement). A similar line of reasoning/approach can be use this paradigm to examine potential appetite suppressant effects. 2.3. Development and gender differences of food protection behaviors Food protection behaviors appear in the behavioral repertoire as early as 20 days of age, shortly after they are able to sit up and hold food (Whishaw, 1988) and perform comparable dodging movements from as early as 15 days postnatally during social play (Pellis et al., 1996). It is stated that laboratory rats only begin to dodge after 5–15 exposures to a robbing attempt, be it by an anesthetized rat, pincher grasp of the experimenter, or a cotton swab tip (Whishaw et al., 1991). Further systematic examination of said learning about the robber would be useful for a variety of paradigms, such as determining if there is a critical period for this experience, whether it differs by strain, sex, or dominance of the individual, if it is influenced by pharmacological manipulations that affect episodic memory, and examining the ability of a single victim to differentiate various robber abilities. Research supports that food protection behaviors are not as influenced by the robber’s approach as they are by other factors. One study independently varied food size and hardness and even whether the robber was allowed to attempt robbing naturally or by manually moving the robber into the robbing position (Whishaw & Gorny, 1994). Their results were consistent with a previous study (Whishaw et al., 1990), concluding that the best predictor of dodge probability and magnitude is the time necessary to complete eating. There is no difference in type of food protection behavior as a function of sex (Whishaw, 1988; Whishaw & Tomie, 1987). However, sex differences exist at the level of motoric organization (Field et al., 1996) resulting in differing orientations towards robbers at the end of a food protection movement (Field, Whishaw, & SM, 1997). Females move away from the robber by using a greater amount of movement of the snout relative to the pelvis than males. To produce the larger amount of hindquarter movement, it was necessary for the males to take more steps with the hind limbs, and males pivoted around a point closer to the midbody, whereas females pivot around a point nearer the pelvis (Field et al., 1996). Kinematically, females attained a greater maximum velocity of the snout relative to the pelvis, as well as a larger temporal separation of the initial peaks in velocity of the snout and pelvis, relative to males. Furthermore, Field and colleagues found that the torso travelled a greater distance and attained a greater velocity than the pelvis relative to the males. The differences in gender were not due to differences in vertical movement during food protection, nor was it due to the behavior of the robber. In fact, irrespective of the sex of the robbing animal, both males and females continue to use sex-typical patterns of pivoting (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997). Several studies further examine the development of sex-typical food protection behaviors. A developmental study conducted by Pellis et al. (1999) investigated the genesis of sex-differentiated motor patterns in food protection behaviors by analyzing male and female victims before and after puberty. Both males and females performed sex-typical versions of the dodging motor pattern regardless of age (Pellis et al., 1999). Castrated male rats at weaning are also reportedly unaffected in their food protection behaviors, further suggesting that sex differences are not related to puberty or aggression (Field et al., 1996). Indeed, sex-typical differences in food protection behaviors are already present around 35 days (prior to puberty) (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997), and sexual differentiation of the skeletal system in rats does not occur until puberty (Bernstein & Crelin, 1967 as reported by Pellis et al., 1999). However, manipulation of gonadal androgens immediately after birth can modify the dodge pattern performed by males and females. Females treated with testosterone propionate are more male-like, whereas males gonadectomized on Postnatal Day 1 are more female-like. In addition, it has been shown that the development of this pattern in males is not dependent on the presence of androgens during the pubertal period (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997). Females ovariectomized neonatally results in dodge patterns that are characterized by aspects of movement and stepping that are more typical of a male pattern of organization, those ovariectomized pre-pubertially displayed both female- and maletypical elements, and those ovariectomized in adulthood showed no change in their typical female elements (Field et al., 2004). Pregnant females, however, use a female-typical pattern of dodging, suggesting that the patterns used by prepubertal ovariectomized females are not due to their increase in body mass (Field et al., 2004). Research on tfm-affected rats further substantiates these findings. Although genetically male with internal testes that secrete testosterone, tfm-affected males are phenotypically female due to a failure of androgen receptor-mediated masculinization of the periphery (Field, Watson, Whishaw, & Pellis, 2005). Although tfm-affected males dodging patterns differed from females, they did not differ from their wild-type male counterparts. Thus, several lines of evidence suggest that the sex differences in dodging patterns are mediated primarily by CNS mechanisms and are not primarily dependent on sex specific skeleto-musculature. The role of social interaction in sex differences has been explored in food protection behaviors. Dominance relationships are established rapidly, which results in a significant decline of within-group fighting. Typically, the animal that is most aggressive in the pretests proved to be the dominant within its colony (e.g., in five of the seven groups tested by Blanchard, Hori, Tom, & Caroline Blanchard, 1988). Pretest offensive levels also influenced behavior of subordinates, with high or moderately aggressive subordinates showing more defensive in interactions with dominants, suggesting that aggression level of the subordinate as well as the dominant may be important factors in determining the intensity of agonistic interactions of male rats (Blanchard et al., 1988). How this relates to food protection remains largely unanswered. Pellis et al. (1999) examined the motor patterns of food protection behaviors in males and females that had been raised with and without Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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social interactions from weaning. Both sexes performed their sex-typical version of the dodging motor patterns; however, orienting to the head of the opponent was disrupted in males reared in social isolation, a feature of dodging that developed between weaning and puberty. Evidence is consistent with the view that while the sexual differentiation of the motor organization of dodging develops without the need for experience, the males’ ability to direct this motor pattern with the correct orientation towards the opponent requires some pre-pubertal experience (Pellis et al., 1999). Evasive lateral movements, similar to food protection behaviors, are frequently performed in other contexts, showing similar gender differences in behaviors such as play fighting (Himmler, Stryjek et al., 2013), isolation induced fighting (Adams, 1976), and sex (Whishaw & Kolb, 1985). Collectively, these results suggest that the sex differences in motor organization are primarily neural based and are not due to differences in skeletal morphology or social interactions (save for the male victim head orientation). Additionally, there are some modifications in the responses of male and female victims based on the gender of the robber (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997). Female victims show a higher frequency in aligning their pelvis with the head of the robber when male, whereas the victim will align her rump with a female robber’s midbody. Male victims align their rump with the head of the male robber yet when there is a female robber, the male will more often align his pelvis with the midbody of the robber. Thus, females switch to a more male-typical alignment and males switch to a more female-typical alignment when paired with opposite sex robbers (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997). These changes do not translate into a gain of additional eating time, but result in the victim ending its food protection behavior with less sensitive body regions aligned with the robber’s snout. This suggests that the variations in responses based on robber gender may be due to male robbers being perceived as more of a threat than female robbers (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997; Whishaw et al., 1990). Although the response is modified based on the gender of the approaching robber, the actual behavior pattern of a dodge is not, suggesting that although extrinsic factors influence aspects of dodging behavior, the dodge patterns are likely due to intrinsic characteristics of each sex (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997). It is interesting to note that all of the studies investigating sex differences focused on behaviors classified as dodging, and new food items were introduced as soon as the behaviors desired were recorded. It would be interesting to see how the transitions from dodging to bracing occur in various dyad gender situations, if magnitude of food protection behaviors vary kinematically, and whether magnitudes vary by food type. 3. Sensory and neural systems involved Research on olfactory, visual, and tactile information in the initiation of food protection behaviors reveal that tactile stimulation produced by the robber when attempting to grasp the food is likely the largest eliciting stimulus of food protection behaviors (Whishaw, 1988; Whishaw & Tomie, 1987). Complete olfactory bulb removal via suction or eye occlusion by black felt patch glued across the eyes do not affect food protection behaviors (Whishaw, 1988). Vibrissae removal produces a transitory change in dodging and bracing where animals will run forward instead of dodge when approached ipsilateral to the side of vibrissae removal, but by three days of testing, responses return to normal type and frequency. A combination of olfactory and vibrissae removal and eye occlusion produce no changes different from that of vibrissae removal, suggesting that tactile stimulation is most important of the senses for initiating food protection behaviors. This is supported by separate studies, with bilateral enucleation within the first 8 h of birth resulting in no change in the initiation of food protection behaviors compared to rats with vision (Pellis et al., 1996). When vibrissae were clipped, non-sighted rats initiated food protection behaviors when the distance between the snout of the robber and the mouth of the defender were much closer – albeit both groups (non-sighted and sighted rats with vibrissae clipped) initiated behaviors when the distance was reduced, suggesting that vision may be used to trigger defensive responses in the absence of tactile cues (Pellis et al., 1996). As discussed above, food protection behaviors are complex and consist of chains of a variety of behaviors and cognitions. As such, it provides a unique opportunity to examine real-world contributions of neural systems in the organization of behaviors. Organization of social behavior is even believed to have its own neural circuitry which includes the mesolimbic dopamine system, the amygdala, and areas of the frontal cortex, including the prefrontal cortex (Himmler et al., 2014). Food protection behaviors appear to have additional circuitries involved. Atropine-sensitive theta rhythm and dodging are disrupted by an infusion of a cholinergic antagonist into the medial septum. Prior to the cholinergic blockade, posterior hypothalamic stimulation produced theta rhythm and dodges, even in the absence of a robber, but following the blockade the victim would drop the food and run, suggesting that atropine-sensitive theta rhythm and hippocampal structures to a role in sensory integration and planning for the initiation of movement (Oddie, Kirk, Whishaw, & Bland, 1997). Similarly, cathodal lesions of the fimbria fornix resulted in loss of food 33–57% of the time when approached by a robber (Oddie et al., 2002). On post-lesion day 8, lesioned rats successfully engaged in food protection behaviors 54% of the time, would wait until a fight ensues with the robber for the food 23% of the time, 15% of the time would engage in avoidance behaviors, and in the remaining 8% of time would either drop the food or have it stolen from their mouth or paws. On post-lesion day 7, lesioned animals were more active in open field behavior, used less thigmotaxis, and entered the center of the square of the apparatus more. Authors suggest the deficit could be due to an impairment in the victim’s spatial assessment of its risk for losing food, it may disrupt movement initiation or it may produce a disengage deficit such that the rat is more focused upon eating the food to the detriment of protecting the food by dodging away from the robber (Oddie et al., 2002). Specifically affecting cholinergic neurons, 192 IgG saporin infusions into the medial septum selectively impaired rats’ ability to transition from Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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dodging to bracing, suggesting impaired processing of temporal information (Martin et al., 2008). A double dissociation was reported in this study, where 192 IgG saporin infusions into the nucleus basalis impaired the rats’ ability to protect the food item from theft, while sparing the transition between food protection behaviors of dodging and bracing and time to consume the food item (hazelnut), suggesting an impairment in the ability to sustain or shift attention (Martin et al., 2008). Similarly contributing to timing theories, amphetamine increases the time spent dodging and suppressed bracing behavior. It also increased the distance between heads of the victim and robber at the initiation and termination of dodging behavior. In contrast, haloperidol decreased the time spent dodging, resulted in bracing throughout the session, and produced decreases in the distance between the heads of the victim and robber at both the initiation and termination of bracing behaviors (Wallace et al., 2006). In general, these results support a role for the speed of an internal pacemaker or clock in organizing food protection behaviors. Medial prefrontal and orbital frontal cortex lesions have been examined in the contexts of both play and food protection. Similar to the finding that rats with lesions of the medial prefrontal cortex (mPFC) preferentially use simpler defensive tactics during play fighting (Bell, McCaffrey, Forgie, Kolb, & Pellis, 2009), the mPFC has a role in the coordination of movements with a partner during food protection as well (Himmler et al., 2014). Rats with bilateral mPFC lesions had more food stolen (80% of the time versus 0% for intact rats), and displayed an inability to maintain interanimal distance with partner, but did not exhibit any motor or sensory deficits. Victims with mPFC lesions began to move away from their partner at the same interanimal distance as the control rats but were unable to maintain consistent interanimal distances during dodges. These findings suggest that the reduced ability of the rats with mPFC lesions to defend a food item from a robber is due not to their inability to execute movements in a timely and efficient manner, but because of an impairment in their ability to execute those movements in a way that is properly coordinated with those of their partners (Himmler et al., 2014). In adult rats, the cells of their mPFC show evidence of extensive neural pruning as a result of the rats having had playful interactions in the juvenile period (Bell et al., 2009; Himmler, Stryjek et al. (2013) both as reported in Himmler et al., 2014). Rats with neonatal orbital frontal cortex (OFC) lesions showed persistent social deficits in play fighting, including a hyperactive level of play and an absence of partner-related modulation behaviors. Adult OFC lesions resulted in normal responses to food cues but impaired discrimination of robbers (Pellis et al., 2006). Although these researchers did not examine the effects of neonatal lesions on food protection behaviors, results of such studies would be insightful. 3.1. Unilateral brain damage Unilateral cortical removal in hemidecorticate victims does not impair food protection behaviors when the robber approaches them ipsilateral to their lesion (Whishaw & Tomie, 1988). However, when approached contralateral to their lesion, they initially made no dodges at all for the first 10 days postoperative. They slowly improved over 60 days, ending with an average of food being stolen 69% of the time. Further studies examined specific cortical regions unilaterally. Unilateral six-hydroxydopamine hydrobromide (6-OHDA) lesions resulted in differing impairments based on the side and time post-operatively. Approaches from either side initially resulted in typical food protection behaviors for the first few days following surgery, but after this, ipsilateral approaches resulted in backwards dodges that were described as “far fewer successful dodges. . . . food was seldom stolen, however”, whereas contralateral approaches resulted primarily in standard dodges or the food being stolen (Whishaw & Tomie, 1988). Such impairments persisted in half of the animals at the end of testing, at 60 days whereas the other half of the animals recovered to almost normal. Unilateral cortical lesions of the parietal cortex do not affect food protection behaviors (Whishaw, 1988), whereas unilateral suction ablation to the medial frontal cortex, neocortex, or all neocortex plus medial frontal and cingulate cortex result in temporary disruptions in food protection behaviors when robbers approach contralateral to the lesion. Medial frontal lesions resulted in partial ability to protect food that was restored by day 5 of recovery. In spite of several lines of evidence suggesting the superior colliculus may be involved in food protection behaviors, ibotenic acid lesions and suction removal of the colliculus and overlying cortex did not affect food protection behaviors (Whishaw, 1988). Counterintuitive results of unilateral medial frontal lesions, hemidecorticate, and unilateral dopamine-depleted animals suggest further inquiry may provide novel insights into the character of underlying systems for food protection behaviors (Whishaw, 1988). 4. Robbing behavior There are several dissociations between food protection and robbing behaviors. In contrast to tactile stimulation being most important in the initiation of food protection behaviors, olfaction appears to be most important in robbing behaviors. Complete olfactory bulb removal via the suction method affects robbing behaviors (Whishaw, 1988), suggesting that the robber uses olfactory cues to target its attack on the food. Further differences are observed in lesion studies. For instance, hemidecortication and 6-OHDA lesions result in different impairments in robbers versus victims (Whishaw & Tomie, 1988). Hemidecorticate rats made normal robbery attempts approaching from the side ipsilateral to their lesion, much how they were unimpaired in food protection behaviors ipsilateral to their lesion (Whishaw & Tomie, 1988). However, their contralateral side of the lesion only resulted in a transient impairment that recovered rapidly, within a few days they made normal robbery attempts – a much faster recovery than observed in food protection behaviors. A similar dissociation was reported in unilateral 6-OHDA rats. They were impaired in robbing when approaching from either side but performance was slightly improved when using the side ipsilateral to their Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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lesion. Intrusion of rotational behavior as noted to contribute to their failures in robbery attempts (Whishaw & Tomie, 1988). Another example of differentiation between food protection and robbing, cathodal lesions of the fimbria fornix resulted in impairments in food protection behaviors but not robbing behaviors (Oddie et al., 2002). And finally, unilateral medial frontal cortex suction ablation had minimal effect on robbing, with rats being successful as early as day 1 post-surgery (Whishaw, 1988), whereas neocortex and neocortex with medial frontal and cingulate cortex ablations impaired robbing, although recovery was rapid and nearly complete by day 2. Unlike the multifaceted interactions of extrinsic influences that can influence food protection behaviors (e.g., age, sex, sex of robber, social exposure), robbing behaviors are less understood but again, do appear to fundamentally differ. Approach behavior of the robber, typically a rear oblique angle of approximately 45◦ , does not change with the age or sex of the victim (Pellis et al., 1999). Male robbers initiate attempts sooner than female robbers and social isolation hastens their responses even more, whereas female robbing behavior remains unchanged even if socially isolated. In contrast, research shows that the topography of aggressive behavior of an attacking male rat is determined by the behavior of the male victim when the victim’s behavior was manipulated by pentobarbital and/or shock (Sbordone & Elliott, 1978). Additional studies examining social standing, dominance, and individual propensity may yield more insight. 5. Heuristics Food protection behaviors are multifaceted and offer a great opportunity of study to a variety of fields. Several ideas are proposed here. As reviewed previously, topographic and kinematic analyses of both the victim and robber have been documented and examined as a function of sex and prior social exposure (e.g., Pellis et al., 1999). However, in these analyses, the first five dodges of 135 ◦ are recorded and new food items are provided as needed to obtain the data desired (e.g., Field et al., 1996; Pellis et al., 1999). Further kinematic and topographic analyses of food protection behaviors throughout the consumption of a single food item would provide additional insight into the motor action patterns, the transition from “dodging” to “bracing”, cognitive updating of the animal as it interacts in its environment, and the neural circuitry involved. 5.1. Dodging – through an ethological lens As reviewed in earlier sections, sex differences in dodging patterns are predominately mediated by CNS mechanisms rather than skeleto-musculature (e.g., Field et al., 2005), although the CNS mechanisms by which these sex differences arise remain unanswered. As raised by Field et al. (2004), further research can examine relative contributions of the active ovarian steroids (progesterone, estrogen, or metabolites) and their associated receptor subtypes to the development of female-typical patterns of movement and its neural control. For instance, it has been shown that female hormones, most specifically estrogen, can have influences on the biochemical and behavioral output of dopaminergic (Quesada & Micevych, 2004) and cerebellar–olivary (Smith, 1998) circuitry, both of which are implicated in the coordination of locomotor activity. Dodging can provide insights into the organization of movement. The dodging movements of rats occurs in a variety of behaviors, including sexual (Whishaw, 1988; Whishaw & Kolb, 1985), playful (Himmler, Derksen, Stryjek, Modlinska, & Pisula, 2013; Pellis et al., 2006), aggressive (Pellis & Pellis, 1992), and food-related (Field, Whishaw, & Pellis, 1997; Field, Whishaw, & SM, 1997; Whishaw & Gorny, 1994; Whishaw & Tomie, 1987) social encounters. For instance, dodging is also observed in mating female rats in response to an approaching male or inappropriate contact (Whishaw & Kolb, 1985). This seemingly identical behavior in a different context suggests that this movement unit may be a useful paradigm to study stimulus control of complex behavior and its neural basis. The finding that similar movements occur in dissimilar behavioral sequences (such as in female dodging of inappropriate approaches by males), suggests that the movement unit may be inserted into different chains of behavior as required (Whishaw, 1988). Dodging can be dissociated from orienting and turning because both hemidecorticate and dopamine-depleted (6-OHDA) rats were not able to dodge in a direction ipsilateral to their lesion when approached contralaterally to the lesion, but did show a strong bias to spontaneously turn in that direction, suggesting that orienting and dodging are subserved by different neural systems – perhaps that each hemisphere functions to direct orienting movements contralaterally and dodging movements ipsilaterally (Whishaw & Tomie, 1988). Previous researchers have described how the form of food protection behavior movements is similar to the turning movements described under the conceptual title of the “mobility gradient”, or “warm-up” (Golani, 1992; Whishaw & Gorny, 1994), which may provide the framework for a better understanding of movement order and disorder. According to the mobility gradient theory, head movements of various amplitudes do not occur in isolation; rather, they recruit more caudal body parts to increase the size of movements and are mediated by a family of basal ganglia-thalamocortical circuits and their descending outputs (Golani, 1992). The mobility gradient theory suggest that there are rules of organization common to locomotor development in vertebrates, suggesting that behavior progresses from immobility to increasing complexity and unpredictability (Golani, 1992), and more importantly perhaps, that these component movements can be closely linked to exogenous sensory stimuli in a complex manner (Whishaw & Gorny, 1994). Food protection behavior research supports and extends this theory to suggest that such behaviors can also be elicited by the rat’s estimation of time left to consume the food item, supporting that brain structures that mediate cognitive judgements concerning eating times are linked to brain structures that produce component movements of the mobility gradient (Whishaw & Gorny, 1994). Behavioral descriptions and models of motor adjustments in natural behaviors may be more useful, or at least provide a different lens in which to Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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examine neurological disorders, including but not limited to, consequences of unilateral brain damage and compensation. For instance, Whishaw and Tomie (1988) speculate that the absence of dodging may be characteristic of human patients with Parkinsonism when they brush against a curtain or door when walking and stop suddenly, unable to move. Looking at characteristics of rats in general raises several ethological questions concerning food protection. Given the neophobic nature of rats (Modlinska & Stryjek, 2016), future studies could examine how food protection behaviors are organized when given novel food items in the presence of a conspecific. This could provide insight into a rat’s motivation, or willingness to engage in food protection behaviors by examining the timing of the transition to bracing, the number of thefts, and/or the overall attempt to protect the item. In another vein, suggestions that laboratory rats differ in terms of behavior, morphology, and physiology as a result of domestication (Modlinska & Stryjek, 2016), lead to an interesting question of how food protection behaviors differ among domesticated strains and wild rats. As previously discussed, defense of home regions vary based on strain of rats. Results in studies on play fighting show a similar focus on the neck region. Domestic and wild rats attack and defend the nape during play, a non-agonistic body target (Himmler, Stryjek et al., 2013). However, play is less frequent in wild rats and were less likely to use tactics that promoted bodily contact. None of the research investigating strain differences examined food protection behaviors in terms of dodging and bracing, and many lack detailed kinematic profiles of food protection behaviors. Another interesting consideration is that typically, rats begin eating at the onset of the dark cycle (Barbarich-Marsteller et al., 2013) yet in the studies reviewed for this paper, food protection behaviors were analyzed during the light cycle. Future research should explore how food protection behaviors vary within the species among laboratory strains and wild rats, and among conditions more similar to laboratory versus wild rats. Given the pervasive necessity of obtaining food, it might be expected that the behaviors of food wrenching and dodging would be common to many animals. Whishaw et al. (1998) compared food wrenching and dodging in Long-Evans and Sprague-Dawley rats (Rattus norvegicus) and out-crossed CDF1 and inbred C57b mice (Mus musculus). It would be insightful to analyze which strains and/or species under various conditions engage in food protection behaviors. Interestingly, although mice were never observed to dodge in the plexiglas testing apparatus used commonly for rats, mice displayed similar robbing behavior to that of rats (Whishaw et al., 1998). Mice were also more successful and more likely to pursue and try again, successfully robbing approximately 25% of the time, compared to 1% success rate of rats. When tested in their home case, mice did dodge, but still dodged less and ran away or fought more than rats when consuming food items. This may suggest robbing behaviors are less sophisticated forms of behavior, or that the action patterns associated with robbing is more important for survival. There were no strain differences in rats, but C57b mice dodged less than CDF1 mice, and male mice appeared to dodge less frequently than females (particularly the C57 strain) (Whishaw et al., 1998). Given that dodging is a component not only of food defensive behavior but also of play, sexual, and aggressive behavior, the species and strain differences may be a key element of changes in social behaviors that differentiate rats from other rodents. Additional ethological studies could examine behaviors in similar species to further understand this differentiation. A final ethological thought concerns further research on the robbing behaviors. These behaviors differ greatly from food protection behaviors both neurally and physically, and remain largely unexplored. Research has shown that robbers can learn and take advantage of individual weaknesses, for instance in unilaterally impaired victims (Whishaw & Tomie, 1988). After a little experience in robbing, it was observed that the robber will quickly learn which side is most likely to result in a successful robbery. How the robber makes this discrimination remains unclear. It may be a response to the victim’s behaviors, such as shifts in posture, piloerection, and/or vocalizations (Whishaw & Tomie, 1988). How robbing behaviors compare not only within the species based on individuality, learning, and motivation, but also across species remains to be documented. As mentioned in the previous paragraph, although mice appear to not utilize food protection behaviors to the same extent as rats, they do engage in robbing behaviors and may even be more successful. Although robbing behaviors are fundamentally distinct and more impervious to social change, their organization within and across species remains unexplored. 5.2. Dodging – through a social lens Rats typically live in colonies of mixed genders, and the complexity of their behaviors as influenced by social structure is best examined in realistic scenarios. Males are dominant to females, and males establish dominance among themselves as well. Additionally, Whishaw and Tomie report that food protection behaviors will occur more so in cohabitating than in unfamiliar rats (Whishaw & Tomie, 1987). Dodging behaviors have been reported in a variety of other scenarios beyond food protection, and has been rather extensively documented in play. Rats with neonatal or adult damage to the motor cortex fail to exhibit age-related modulation of playful defense typically present in intact rats (Kamitakahara, Monfils, Forgie, Kolb, & Pellis, 2007). In contrast, male rats with adult orbital frontal cortex ablations were not impaired in protecting their food but they were impaired in their ability to modify the pattern of defense in response to different partners (Pellis et al., 2006). Bilateral damage at 3 days of age also resulted in impaired ability to defend themselves during play as well as hyperactivity in play (although neonatal lesions on food protection behaviors were not examined) (Pellis et al., 2006). Such damage also disrupts the rats’ ability to modify its social behavior non-playful contexts as well (Kamitakahara et al., 2007), suggesting that the role of the OFC is in modulating behavior patterns in socially significant contexts rather than in the production of behavior patterns. Neonatal ablations of the mPFC resulted in fewer playful responses to playful attacks, and more evasions (Bell et al., 2009). Is it due to impaired temporal sequence responses because social play is a dynamic activity requiring the behavioral response of one animal to the behavioral input from another? Medial prefrontal cortex lesions produce a shift from more Please cite this article in press as: St. Peters, M.M.M. Insights from rodent food protection behaviors. Learning and Motivation (2017), http://dx.doi.org/10.1016/j.lmot.2017.01.004

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complex to less complex defensive tactics, while leaving age-related and partner-related modulation of defensive strategies in play fighting, suggesting a triple dissociation of function between the MC, OFC, and mPFC with respect to social play behavior (Bell et al., 2009). Specifically, the changes in play produced by complete neonatal decortication can be explained by OFC lesions that abolish normal, partner-related modulation of defensive tactics (Pellis & Pellis, 1992), the MC lesions eliminate normal, age-related modulation in defensive tactics (Kamitakahara et al., 2007). In contrast, mPFC lesions leave both these intact but disrupts the organization of the movements used in play (Bell et al., 2009). These findings are consistent with the view that the mPFC is involved in regulating the selection and execution of complex behaviors (Bell et al., 2009). Studies such as these reveal the importance of examining social behaviors and their related neural activity in complex, “real world” scenarios. Interacting with conspecifics is typical for many social species, such as humans and rats. As such, modulation of food protection behaviors in rats provides a potentially useful model for exploring the mechanisms by which such social skills are developed and subject to modification with experience. Indeed, the juvenile period is a critical time for the development of social behaviors with conspecifics, and may be important for the development of behavioral flexibility and emotional regulation (as reviewed in Himmler et al., 2014). During the juvenile period, rats that do not actively engage in social interactions with their peers are impoverished in their ability to coordinate movements with social partners and fail to prune the dendritic arbor of neurons of the medial prefrontal cortex (reviewed in Himmler et al., 2014). Human children with autism spectrum disorder (ASD), a condition known to be associated with mPFC abnormalities, show patterns of social behavior similar to those observed in the mPFC ablated rats (Bell et al., 2009). The range of impairments in ASD or even general social behavior varies widely among individuals. As food protection behavior is a rather quick yet cognitively and socially complex paradigm, it may prove useful as a paradigm for identifying risk factors for social delays or impairments in individual vulnerabilities. 6. Final thoughts In conclusion, food protection behaviors allow for the “basic and applied analysis of defensive and aggressive behavior” (Whishaw & Gorny, 1994) and more. At its simplest, food protection behaviors involve spatial knowledge of oneself in relation to a conspecific, ability to anticipate the likelihood and speed of a robber’s approach, interval timing estimates of consumption time of food item remaining to determine magnitude of food protection behavior, motor initiation and organization of behaviors, and general attention and motivation. Research continuing to unravel the neural organization of food protection behaviors contributes to a variety of fields and can be interpreted from a variety of perspectives, such as ethological, evolutionary, developmental, neural, and social. Food protection behaviors not only provides a context in which to examine underlying systems of interest to better understand the species, but also as an antecedent for understanding human behaviors and conditions. 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