Encoding of local and global cues in domestic dogs’ spatial working memory ()
1. INTRODUCTION
In most animals, the ability to solve spatial problems is essential for survival. For example, remembering the location of a food cache or traveling from and to nest (or home) are some of the basic spatial problems encountered by animals on a daily basis. Over the years, comparative researchers have extensively investigated spatial cognition and have reported the use of several cues and mechanisms in the spatial domain by animals (for a review see [1-4]).
Although animals can encode and use multiple sources of spatial information to remember and locate a spatial position, these sources can be roughly grouped into two categories: egocentric and allocentric cues [5]. Egocentric cues refer to the information provided by the spatial coordinates of the animal and its own movements through space [6]. Two forms of egocentric information have been identified. In its simplest form, which is called linear egocentric information, the animal plans and maintains from its starting position a direct path towards a specific location. A most complex form of egocentric information refers to dead reckoning (also known as path integration). This latter is used by animals to keep track of their displacements in space by encoding inertial information such as direction, distance and speed. However, egocentric spatial information is inflexible: if the relationship between the animal’s position and the target location is broken (e.g. by the introduction of an obstacle that forces the animal to deviate from its planned trajectory), egocentric information would orient the animal towards an incorrect location. As for it, allocentric spatial information refers to the relationships between a specific location and the objects surrounding it [6-9]. Examples of allocentric cues are trees or rocks that can be used by the animal to record a location. By contrast to egocentric information, allocentric cues provides a flexible source of information because an animal can reach its target location by following different routes and reorient itself by using one or several familiar objects in the environment. Allocentric information is therefore extremely helpful when the desired location cannot be perceived directly from the starting position of the animal [10].
In domestic dogs, the study of spatial cognition is still at the embryonic form. One of the first studies to be conducted in domestic dogs is described by Carthy [11]. In this study, the dogs were released 6 km from their owner’s house and their task was to walk back to their home. Over trials, the dogs gradually learned to reorient from the release point in direction to their home and to use a shorter route. Although this study suggests that dogs are able to use allocentric cues (e.g. roads, trees, etc.) to navigate within a familiar environment, it does not provide any cues about the nature of the spatial information encoded by the dogs. In a study aimed at investigating whether dogs encode egocentric or allocentric cues, Chapuis [12] used a returning task. In this experimental situation, the dog was first led along an outer path to a piece of food placed inside a bowl but the dog was refused to eat. Then, the dog was led along the same direct path to a choice point. From this position, six similar bowls (including the target one) were disposed in a semi-circle. The dog’s task was to walk back to the target bowl. After several days of training, the dogs were tested in various situations: the distance between the bowl was altered, the number of bowls was doubled, the bowls were shifted to a new spatial location in the outdoor area, the dogs were carried to the choice point or the outer path was covered by a tunnel. Overall, the results suggested that dogs prefer to use allocentric cues rather than egocentric cues to return to a food location. For instance, when the bowls were translated to a new spatial position or if the number of bowls was doubled, the dogs’ performance dropped significantly. However, when the egocentric frame of reference was broken, the dogs’ performance was still very good. In another study [13], the dogs had to bypass two opaque or two transparent screens forming a V-shaped panel to reach a food cache (bowl). In this particular study, the length and the angle of the detour were manipulated by varying the length and position of the panel placed between the animal and the food. The results revealed that if the bowl of food was visible from the starting position, the dogs used egocentric cues and ignored the distance. However, if an opaque panel blocked the visibility of the bowl, the dogs encoded an allocentric representation and used the shortest path to reach the food. On the other hand, when their eyes are blindfolded in a search task, dogs can also rely on dead reckoning by keeping track of their displacements and reorientations in space [14]. Put together, these pioneer studies on dogs’ spatial cognition suggested that dogs, like several other species, can encode and use both egocentric and allocentric cues.
More recently, Fiset and his colleagues have used an object permanence task to investigate whether dogs encode egocentric or allocentric cues in spatial working memory to navigate. More specifically, spatial working memory refers to remembering properties of locations in working memory over a short period of time. In this task (called “visible displacement problem”), which was initially developed by Jean Piaget [15] in human children, an attractive object (e.g. toy, ball) is visibly hidden behind one of several identical locations (usually three or four) and a few seconds later the animal must remember and locate the hiding position of the object. From trial to trial, however, the target object is hidden behind a different location, forcing the subject to rely on working memory to memorize different properties of locations to find the hidden object. Since several animal species face situations in which objects move and disappear (e.g. prey), the visible displacement problem is well adapted to investigate spatial working memory in animals.
The previous studies by Fiset and his colleagues showed that if there is a linear trajectory between the dog’s encoding position and the position of the hidden object, the dog primarily uses egocentric cues. Most specifically, dogs encode a directional vector (including distance and direction) that starts at the animal’s position and points toward the target location [6], supporting the previous work by Chapuis and her colleagues [13] in a different spatial task. However, the use of a direct path toward the hidden location is not always possible. For instance, the dog may have to bypass a brush or a pound before reaching the hiding location. By consequence, Fiset, Beaulieu, LeBlanc and Dubé [16] recently investigated spatial working memory of domestic dogs for hidden objects in a detour paradigm (for a similar approach in chicks, see [17,18]). Results revealed that dogs simultaneously encode both dead reckoning and allocentric spatial information when they have to bypass an obstacle to locate a hidden object. Besides when the detour involved several reorientations (U-shaped detour), over the course of time, the dogs gradually learned to rely exclusively on allocentric cues and abandoned the use of dead reckoning. This latter experiment, however, does not provide any clues about the nature of the allocentric information that is encoded in dogs’ spatial working memory.
Animals mainly use two sources of allocentric spatial information to navigate: local and global cues [10,19-23]. Local cues are usually designed as objects, such as rocks, logs, or featural cues (e.g. colors) that directly marked the exact location of the desired location [21] or that are located in the vicinity of the cache [10]. As for them, global cues refer to objects that lay at a distance from the target location. In an open environment, global cues may be distant objects, such as mountains or the tree line, whereas in an enclosed space (e.g. a testing room), the geometric relationships of walls refer to the global geometry of the room and they are also frequently termed as global cues. It is usually assumed that global cues guide the animal toward a specific area whereas local cues are used as beacons to pinpoint a specific position within this area [24]. However, some authors assume that relationships between the global cues can also be use to pinpoint the animal towards a specific location [21].
There is evidence that animals are more sensitive to one allocentric cue than the other. For instance, in his classic studies on rats’ spatial representation, Cheng [24] demonstrated that rats remembered a target location by using the global geometry of an enclosure and did not use the featural cues (local cues) added to the enclosure. Spetch and Edwards [22], however, found that in pigeons, local cues largely dominated global cues. Interestingly, when either local or global cues were made unavailable, pigeons relied on the alternative source of information to locate the food, suggesting that pigeons hierarchically encode spatial information: local cues dominate but global cues are also simultaneously encoded and used if necessary. Vallortigara, Zanforlin and Pasti [25] found a similar but inverse conclusion: Chicks could encode and use geometric (global) and featural (local) information but primarily rely on featural information when both cues are available. Readers are invited to consult Spetch and Kelly [26] who elegantly summarized how animals encode and use both local and global cues in various experimental settings.
To address the question of whether animals encode local or global cues to navigate, the landmark-based search paradigm is often used [26,27]. In this approach, an animal is trained to locate a piece of food hidden at a fixed distance and direction from one landmark or an array of landmarks within a large environment (e.g. a testing room). After training, the landmark or the array of landmarks is systematically shifted to a new location in the room, putting into conflict the vectors (distance and direction) emanating from the landmark (or from the array of landmarks) and those emanating from the walls of the room. Although pioneer works [20,28,29] suggested that birds encode distance and direction from individual vectors from landmarks only, later work by GouldBeierle and Kamil [30] suggested that birds could also encode vectors from the walls of the room. In this study, Clark’s nutcrackers were trained to locate a target location between two local landmarks. On tests, although the landmarks were removed from the room and that the closest wall was located 110 cm from the target position, the birds still accurately located the target position.
Fiset [31,32] used the landmark-based search paradigm to investigate whether dogs encode the distance and direction from local and global cues. In these studies, a ball was hidden under a layer of woodchip located near one or two particular landmarks (a cylinder) or one or two walls. On tests, the landmark(s) was (were) shifted laterally, perpendicularly or diagonally relative to the walls of the testing chamber. The results showed that dogs encoded both the distance and the direction from the landmarks (local cues) and the walls (global cues), suggesting that they simultaneously encoded both sources of spatial information and attempted to average the vectors emanating from each cue. However, given that the landmark-based search task is a reference spatial memory paradigm (the spatial location of the hidden object is the same from trial to trial so that the information is encoded in long term memory), it still remains to determine whether dogs encode both local and global cues for a short period of time in spatial working memory.
In the current study, we used an object permanence task to investigate the nature of allocentric spatial information (local vs global cues) encoded in dogs’ spatial working memory. To reach this objective, the current experiment took place in the same experimental room used by Fiset et al. [16]. In this experimental setup, the experimenter who manipulated the object and the boxes used to hide the object were termed local cues. As for them, the walls of the searching room referred to global cues. The dogs were first trained to use allocentric spatial information to find a target location in a U-shaped detour task. In tests, local and global cues were systematically put in conflict to determine which of these two sources dogs predominantly used. If dogs were primarily encoding local cues, they should have encoded the hiding position by relationships to the experimenter’s position and/ or the position of the other nontarget boxes. If the dogs were encoding global cues, however, they should have searched as a function of the relationships between the walls of the searching room and the target box.
2. MATERIAL AND METHODS
2.1. Animals
The animals were seven purebred adult Labrador retrievers (4 females and 3 males; mean age = 4 years and 10 month, range = 3 - 9 years) that belonged to private owners. All dogs had already participated in an object permanence study, but they were all naive to the detour task used in the present experiment.
2.2. Material
Figure 1 illustrates the experimental room (362 cm wide × 604 cm deep), which was separated in two parts by a vertical low wall (305 cm wide × 122 cm high). One part of the room (362 cm wide × 250 cm deep) served as the searching room where the target object was hidden by E1 (Experimenter 1). The dog and E2 (Experimenter 2) were located in the second part of the room (362 cm wide × 354 cm deep). The dog sat in front of an opening (85 cm high × 57 cm wide) made in the vertical wall, and E2 knelt at the left side of the dog. The center of this