Behavioral and neural subsystems of rodent exploration
Introduction
Animals occupy territories in which resources such as food and shelter are often distributed unevenly. Given the challenges involved in securing resources while at the same time minimizing the risk of predation, it is critical that animals optimize their movements to efficiently explore the space. While studies of exploratory behavior have been conducted in a wide number of animal species (Berlyne, 1960, Menzel, 1973, Renner, 1990), research involving the laboratory rodent as an experimental subject has largely dominated the field (Barnett, 1963; Drai, Kafkafi, Benjamini, Elmer, & Golani, 2001; Eilam and Golani, 1989, Whishaw and Whishaw, 1996). The concentration on rodent research stems from the fact that their exploratory activity can be assessed in a variety of test situations including multi-choice mazes, cylinders, open-fields, and in response to brain manipulation (Clark, Hines, Hamilton, & Whishaw, 2005; File, 1985; Gharbawie, Whishaw, & Whishaw, 2004; Hall, 1934, O'Keefe and Nadel, 1978, Renner, 1990, Whishaw, 1974). An additional advantage of using rodents as subjects for experimental study is that, although behavior is variable from animal to animal, some movements are identifiable across tasks and rodent species. For instance, orientation responses towards environmental stimuli have been well characterized (Pavlov, 1927, Sokolov, 1963). Other movements that can be readily measured include the vertical movements made by animals when rearing up on their hind legs or against surfaces (Gharbawie et al., 2004; Lever, Burton, & O'Keefe, 2006), and general locomotor activity that takes an animal from one location to another (O'Keefe & Nadel, 1978).
Nevertheless, several challenges to the quantification of exploratory behavior remain. For example, rodent exploratory movements are often described as stochastic or random, and lacking moment-to-moment consistency (Morris, 1983, Tchernichovski and Golani, 1995). Others have argued that rodent behavior in open-fields and complex mazes are difficult to describe quantitatively, and much of the focus has remained on simple end-point measures such as the cumulative distance traveled, the number of photobeam crossings during a test, and locomotor speed. A second difficulty in quantification is whether exploratory behavior should be formulated in terms of the movements involved (Teitelbaum, Schallert, DeRyck, Whishaw, & Golani, 1980), or in relation to the underlying motivations or goals (Morris, 1983, Renner, 1990; Whishaw, Gharbawie, Clark, & Lehmann, 2006). Indeed, exploratory activity is often described in terms of concepts such as fear and anxiety (Blanchard, Kelly, & Blanchard, 1974; Gray, 1982, Montgomery, 1955, Russell, 1973), curiosity and information-gathering (Berlyne, 1960), and the acquisition of spatial “maps” of the environment (Nadel, 1991, O'Keefe and Nadel, 1978).
A recent line of investigation has utilized a descriptive approach to the study of rodent exploratory behavior, which involves breaking the movements down into simpler behavioral subsystems which, when recombined, reconstitute the original full pattern of exploratory behavior (Golani, 2012, Teitelbaum et al., 1980; Whishaw, Cassal, & Majchrzak, 1994). Such descriptions have revealed that the structure of exploration is far from random, and is composed of movement subsystems that can be readily quantified (Eilam and Golani, 1989, Golani, 2012; Golani, Benjamini, & Eilam, 1993; Hines & Whishaw, 2005; Wallace, Hines, Pellis, Whishaw, 2002; Wallace, Hines, Whishaw, 2002; Whishaw, Hines, & Wallace, 2001). In this review, we describe some of the central features of this organized behavior pattern. Much of our discussion will center on the observation that rodent exploratory behavior is organized around specific environmental locations termed “home bases” (Chance and Mead, 1955, Eilam and Golani, 1989). It has been argued that home bases serve as an organizational feature of rodent locomotor activity from which exploratory trips or excursions are made into the remaining environment. Although this rodent behavior pattern appears early in development and is likely a behavioral primitive (Loewen, Wallace, & Whishaw, 2005), the organization of these movements can be modulated by sensory cues as well as previous experience with environment stimuli (Clark et al., 2005; Lehmann, Clark, & Whishaw, 2007). We conclude this review by summarizing work on the neurobiological bases of rodent exploration, which we hope will stimulate renewed interest and organize future thinking for the study of exploratory behavior.
Section snippets
Rat home base behavior
Early studies investigating the exploratory movements of rodents have remarked on the natural tendency of animals to establish preferred “home” locations from which they make excursions into the remaining environment (Chance & Mead, 1955). For instance, feral rats maintain home burrows from which they organize their foraging and avoidance of predation (Barnett, 1963, Whishaw and Whishaw, 1996). Eilam and Golani (1989) provided one of the first experimental characterizations of home base
Neural subsystems in rodent exploratory behavior
Very little is known regarding the neurobiological mechanisms of exploratory behavior. The organized patterns described in the previous sections however lends itself uniquely to measuring the effects of brain manipulations on exploration. Further, if exploration is a mechanism for the acquisition of environmental information, then studies of spatial memory could benefit from a better understanding of the neural basis of these movement subsystems. Indeed, the relationship between exploratory
General conclusion
In the present review, we have summarized a large body of work directed toward understanding the movement subsystems involved in rodent exploratory behavior. We present extensive evidence suggesting that rodents readily establish home bases, defined as regionally restricted bouts of grooming, rearing, tight turning, and long duration stops (Eilam and Golani, 1989, Wallace and Whishaw, 2003). The home base therefore acts as a central feature of the organized pattern of exploratory movements made
Acknowledgment
This manuscript was written while the authors were supported by grants from NIAAA (P50AA022534 and R21AA024983).
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