Growing in circles: rearing environment alters spatial navigation in fish

ABSTRACT— Animals of many species use the geometric shape of an enclosed rectangular environment to reorient, even in the presence of a more informative featural cue. Manipulating the rearing environment affects performance on spatial tasks, but its effect on the use of geometric versus featural navigational cues is unknown. Our study varied the geometric information available in the rearing environment (circular vs. rectangular rearing tanks) of convict cichlids ( Archocentrus nigrofasciatus ) and tested their use of navigational cues. All the fish used geometric information to navigate when no features were present. When features were present, the fish used geometric and featural information separately. If cues were in conflict, fish raised in a circular tank showed significantly less use of geometric information than fish raised in a rectangular tank. Thus, the ability to use geometry to navigate does not require exposure to angular geometric cues during rearing, though rearing environment affects the dominance of featural and geometric cues.     

Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish

When disoriented in environments with distinctive geometry, such as a closed rectangular arena, human infants and adult rats reorient in accord with the large-scale shape of the environment, but not in accord with nongeometric properties such as the colour of a wall. Human adults, however, conjoined geometric and nongeometric information to reorient themselves, which has led to the suggestion that spatial processing tends to become more flexible over development and evolution. We here show that fish tested in the same tasks perform like human adults and surpass rats and human infants. These findings suggest that the ability to make use of geometry for spatial reorientation is an ancient evolutionary tract and that flexibility and accessibility to multiple sources of information to reorient in space is more a matter of ecological adaptations than phylogenetic distance from humans.     

Geometric modules in animals' spatial representations: a test with chicks (Gallus gallus domesticus)

Recent work has shown that in place-finding tasks rats rely on the geometric relations between the goal object and the shape of the environment. We tested young chickens (Gallus gallus domesticus) on similar tasks in a reference memory paradigm to determine whether differences exist between species in the ability to use geometric and nongeometric spatial information. The main findings were that chicks: (a) encoded and used both geometric and nongeometric (featural) information; (b) did not use the overall spatial arrangement of the features; (c) relied primarily on nongeometric cues when faced with contradictory information. Two mechanisms are evident in chicks' spatial representations: a metric frame for encoding the spatial arrangement of surfaces as surfaces and a cue-guidance system for encoding conspicuous landmarks near the target. The possibility of hierarchical organization and species differences in these two mechanisms are discussed.     

Reorientation by geometric and landmark information in environments of different size

It has been found that disoriented children could use geometric information in combination with landmark information to reorient themselves in large but not in small experimental spaces. We tested domestic chicks in the same task and found that they were able to conjoin geometric and nongeometric (landmark) information to reorient themselves in both the large and the small space used. Moreover, chicks reoriented immediately when displaced from a large to a small experimental space and vice versa, suggesting that they used the relative metrics of the environment. However, when tested with a transformation (affine transformation) that alters the geometric relations between the target and the shape of the environment, chicks tended to make more errors based on geometric information when tested in the small than in the large space. These findings suggest that the reliance of the use of geometric information on the spatial scale of the environment is not restricted to the human species.     

Experience and geometry: controlled-rearing studies with chicks

Animals can reorient making use of the geometric shape of an environment, i.e., using sense and metric properties of surfaces. Animals reared soon after birth either in circular or in rectangular enclosures (and thus affording different experiences with metric properties of the spatial layout) showed similar abilities when tested for spatial reorientation in a rectangular enclosure. Thus, early experience in environments with different geometric characteristics does not seem to affect animals’ ability to reorient using sense and metric information. However, some results seem to suggest that when geometric and non-geometric information are set in conflict, rearing experience could affect the relative dominance of featural (landmark) and geometric information. In three separate experiments, newborn chicks reared either in circular- or in rectangular-shaped home-cages were tested for spatial reorientation in a rectangular enclosure, with featural information provided either by panels at the corners or by a blue-coloured wall. At test, when faced with affine transformations in the arrangement of featural information that contrasted with the geometric information, chicks showed no evidence of any effect of early experience on their relative use of geometric and featural information for spatial reorientation. These findings suggest that, at least for this highly precocial species, the ability to deal with geometry seems to depend more on predisposed mechanisms than on learning and experience after hatching.     

Reorientation in a two-dimensional environment: I. Do adults encode the featural and geometric properties of a two-dimensional schematic of a room?

Adults searched for a goal in images of a rectangular environment. The goal's position was constant relative to featural and geometric cues, but the absolute position changed across trials. Participants easily learned to use the featural cues to find the target, but learning to use only geometric information was difficult. Transformation tests revealed that participants used the color and shape of distinct features to encode the goal's position. When the features at the correct and geometrically equivalent corners were removed, participants could use distant features to locate the goal. Accuracy remained above chance when a single distant feature was present, but the feature farthest from the goal yielded lower accuracy than one closer. Participants trained with features spontaneously encoded the geometric information. However, this representation did not withstand orientation transformations.     

儿童空间再定向的几何模块论及其局限

儿童的空间再定向指的是迷失方向的儿童在空间中重新确定自己方位并找回被藏物体的能力。儿童的这一能力与某些低等哺乳动物（如大鼠）相似,都只能利用空间环境所构成的几何信息,不能利用非几何信息来再定向。几何模块论认为造成这一现象的原因是儿童与低等哺乳动物的认知系统里存在几何模块。然而,众多研究对这种简单化的观点提出了异议。针对这些异议,几何模块论又进行了新的修订     

Toddlers' use of metric information and landmarks to reorient

Mobile organisms can keep track of spatial location (both their own location and that of objects in the environment) using either an external referent system or one centered on the self and updated by information about movement through space. When the latter system is disabled (e.g., by rapid turning), aspects of the external world must be used to reestablish orientation. Recently, it has been claimed that, both for rats and for human toddlers, reorientation is achieved using a geometric module that accepts only information about the metric properties of the environment (C. R. Gallistel, 1990; L. Hermer & E. S. Spelke, 1994, 1996). In a series of experiments, this paper confirms that geometric information is used for reorientation by young children, but gives reason to doubt that the use of this information is achieved using a module impenetrable to nongeometric information.     

Is there an innate geometric module? Effects of experience with angular geometric cues on spatial re-orientation based on the shape of the environment

Non-human animals and human children can make use of the geometric shape of an environment for spatial reorientation and in some circumstances reliance on purely geometric information (metric properties of surfaces and sense) can overcome the use of local featural cues. Little is known as to whether the use of geometric information is in some way reliant on past experience or, as would likely be argued by advocates of the notion of a geometric module, it is innate. We tested the navigational abilities of newborn domestic chicks reared in either rectangular or circular cages. Chicks were trained in a rectangular-shaped enclosure with panels placed at the corners to provide salient featural cues. Rectangular-reared and circular-reared chicks proved equally able to learn the task. When tested after removal of the featural cues, both rectangular- and circular-reared chicks showed evidence that they had spontaneously encoded geometric information. Moreover, when trained in a rectangular-shaped enclosure without any featural cues, chicks reared in rectangular-, circular-, or c-shaped cages proved to be equally able to learn and perform the task using geometric information. These results suggest that effective use of geometric information for spatial reorientation does not require experience in environments with right angles and metrically distinct surfaces, thus supporting the hypothesis of a predisposed geometric module in the animal brain.     

Spatial reorientation: the effects of space size on the encoding of landmark and geometry information

The effects of the size of the environment on animals’ spatial reorientation was investigated. Domestic chicks were trained to find food in a corner of either a small or a large rectangular enclosure. A distinctive panel was located at each of the four corners of the enclosures. After removal of the panels, chicks tested in the small enclosure showed better retention of geometrical information than chicks tested in the large enclosure. In contrast, after changing the enclosure from a rectangular-shaped to a square-shaped one, chicks tested in the large enclosure showed better retention of landmark (panels) information than chicks tested in the small enclosure. No differences in the encoding of the overall arrangement of landmarks were apparent when chicks were tested for generalisation in an enclosure differing from that of training in size together with a transformation (affine transformation) that altered the geometric relations between the target and the shape of the environment. These findings suggest that primacy of geometric or landmark information in reorientation tasks depends on the size of the experimental space, likely reflecting a preferential use of the most reliable source of information available during visual exploration of the environment.     

Influence of distal and proximal cues in encoding geometric information

Vertebrates use geometric and featural information for spatial navigation. When both geometric and featural cues are available, animals can use a variety of spatial strategies based on this information. To examine the nature of these strategies, we manipulated the spatial relationship between a conspicuous cue and the position of the goal when goldfish (Carassius auratus) were searching for the exit of a rectangular environment with one distinctive wall. Two groups of fish were used, one with the distinctive wall close to the goal and the other with the distinctive wall on the other end of the enclosure. Results showed that fish encoded featural and geometric information in both conditions but the spatial relationship between the goal and the distinctive wall influences the characteristics of the encoding of the spatial cues and the strategy used to locate the goal. These results suggest that fish in both procedures use the local featural cues associated with the goal instead of the whole set of spatial cues as previous studies propose.     

Individual differences in using geometric and featural cues to maintain spatial orientation: Cue quantity and cue ambiguity are more important than cue type

Two experiments explored the role of environmental cues in maintaining spatial orientation (sense of selflocation and direction) during locomotion. Of particular interest was the importance of geometric cues (provided by environmental surfaces) and featural cues (nongeometric properties provided by striped walls) in maintaining spatial orientation. Participants performed a spatial updating task within virtual environments containing geometric or featural cues that were ambiguous or unambiguous indicators of self-location and direction. Cue type (geometric or featural) did not affect performance, but the number and ambiguity of environmental cues did. Gender differences, interpreted as a proxy for individual differences in spatial ability and/or experience, highlight the interaction between cue quantity and ambiguity. When environmental cues were ambiguous, men stayed oriented with either one or two cues, whereas women stayed oriented only with two. When environmental cues were unambiguous, women stayed oriented with one cue.     

Rhesus monkeys use geometric and nongeometric information during a reorientation task

Rhesus monkeys (Macaca mulata) were subjected to a place finding task in a rectangular room perfectly homogeneous and without distinctive featural information. Results of Experiment 1 show that monkeys rely on the large-scale geometry of the room to retrieve a food reward. Experiments 2 and 3 indicate that subjects use also nongeometric information (colored wall) to reorient. Data of Experiments 4 and 5 suggest that monkeys do not use small angular cues but that they are sensitive to the size of the cues (Experiments 6, 7, and 8). Our findings strengthen the idea that a mechanism based on the geometry of the environment is at work in several mammalian species. In addition, the present data offer new perspectives on spatial cognition in animals that are phylogenetically close to humans. Specifically, the joint use of both geometric and landmark-based cues by rhesus monkeys tends to demonstrate that spatial processing became more flexible with evolution.     

Reorientation in a two-dimensional environment: II. Do pigeons (Columba livia) encode the featural and geometric properties of a two-dimensional schematic of a room?

Pigeons (Columba livia) searched for a hidden target area in images showing a schematic rectangular environment. The absolute position of the goal varied across trials but was constant relative to distinctive featural cues and geometric properties of the environment. Pigeons learned to use both of these properties to locate the goal. Transformation tests showed that pigeons could use either the color or shape of the features, but performance was better with color cues present. Pigeons could also use a single featural cue at an incorrect corner to distinguish between the correct corner and the geometrically equivalent corner; this indicates that they did not simply use the feature at the correct corner as a beacon. Interestingly, pigeons that were trained with features spontaneously encoded geometry. The encoded geometric information withstood vertical translations but not orientation transformations.     

How fish do geometry in large and in small spaces

It has been shown that children and non-human animals seem to integrate geometric and featural information to different extents in order to reorient themselves in environments of different spatial scales. We trained fish (redtail splitfins, Xenotoca eiseni) to reorient to find a corner in a rectangular tank with a distinctive featural cue (a blue wall). Then we tested fish after displacement of the feature on another adjacent wall. In the large enclosure, fish chose the two corners with the feature, and also tended to choose among them the one that maintained the correct arrangement of the featural cue with respect to geometric sense (i.e. left-right position). In contrast, in the small enclosure, fish chose both the two corners with the features and the corner, without any feature, that maintained the correct metric arrangement of the walls with respect to geometric sense. Possible reasons for species differences in the use of geometric and non-geometric information are discussed.     

The Hemispheric Lateralization for Processing Geometric Word/Shape Combinations: The Stroop-Shape Effect

The authors conducted 4 experiments to test whether hemispheric lateralization occurs for the processing of geometric word–shape combinations. In 3 experiments, participants responded to geometric shapes combined with geometric words (square, circle, triangle). In the 4th experiment, stimuli were combinations of geometric shapes and nongeometric words. The authors predicted that it would take longer to respond in incongruent conditions (e.g., the word “square” combined with the shape of a circle) than in congruent conditions. The authors found the strongest incongruency effects for the dominant hemisphere—that is, the left hemisphere for responding to words and the right hemisphere for responding to shapes. A Shape Interfering Properties hypothesis (SIP) is a possible explanation for these results.     

Animals' use of landmarks and metric information to reorient: effects of the size of the experimental space

Disoriented children could use geometric information in combination with landmark information to reorient themselves in large but not in small experimental spaces. We tested fish in the same task and found that they were able to conjoin geometric and non-geometric (landmark) information to reorient themselves in both the large and the small space used. Moreover, fish proved able to reorient immediately when dislocated from a large to a small experimental space and vice versa, suggesting that they encoded the relative rather than the absolute metrics of the environment. However, fish tended to make relatively more errors based on geometric information when transfer occurred from a small to a large space, and to make relatively more errors based on landmark information when transfer occurred from a large to a small space. The hypothesis is discussed that organisms are prepared to use only distant featural information as landmarks.     

Reorientation in diamond-shaped environments: encoding of features and angles in enclosures versus arrays by adult humans and pigeons (Columbia livia)

Although geometric reorientation has been extensively studied in numerous species, most research has been conducted in enclosed environments and has focused on use of the geometric property of relative wall length. The current studies investigated how angular information is used by adult humans and pigeons to orient and find a goal in enclosures or arrays that did not provide relative wall length information. In enclosed conditions, the angles formed a diamond shape connected by walls, whereas in array conditions, free-standing angles defined the diamond shape. Adult humans and pigeons were trained to locate two geometrically equivalent corners, either the 60° or 120° angles. Blue feature panels were located in the goal corners so that participants could use either the features or the local angular information to orient. Subsequent tests in manipulated environments isolated the individual cues from training or placed them in conflict with one another. In both enclosed and array environments, humans and pigeons were able to orient when either the angles or the features from training were removed. On conflict tests, female, but not male, adult humans weighted features more heavily than angular geometry. For pigeons, angles were weighted more heavily than features for birds that were trained to go to acute corners, but no difference in weighting was seen for birds trained to go to obtuse corners. These conflict test results were not affected by environment type. A subsequent test with pigeons ruled out an interpretation based on exclusive use of a principal axis rather than angle. Overall, the results indicate that, for both adult humans and pigeons, angular amplitude is a salient orientation cue in both enclosures and arrays of free-standing angles.     

Adult but not aged C57BL/6 male mice are capable of using geometry for orientation

Geometry, e.g., the shape of the environment, can be used by numerous animal species to orientate, but data concerning the mouse are lacking. We addressed the question of whether mice are capable of using geometry for navigating. To test whether aging could affect searching strategies, we compared adult (3- to 5-mo old) and aged (20- to 21-mo old) C57BL/6 male mice. We established a water maze task in which spatial information is provided by one landmark proximal to the target (featural information) and by the rectangular shape of the maze (geometric information). By means of probe trials in which we manipulated the presence of these two kinds of information, we show that adult mice can use both geometry and landmark to orientate. By contrast, aged mice do not use geometry and rely exclusively on the landmark to locate the platform. This study provides the first evidence that mice are capable of using geometric information for orientation and that this ability declines in aged animals.     

Encoding of geometric and featural spatial information by goldfish (Carassius auratus)

Goldfish (Carassius auratus) were trained in different place-finding tasks as a means of analyzing their ability to encode the geometric and the featural properties of the environment. Results showed that goldfish could encode and use both geometric and featural information to navigate. Goldfish trained in a maplike, or relational, procedure encoded both types of information in a single representation. In contrast, fish trained in a directly cued procedure developed 2 independent and competing strategies. These results suggest that the geometric properties of the spatial arrangement and discrete landmarks are sensitive to encoding in a maplike or relational system, whereas different sources of spatial information are encoded in a single and flexible representation of the environment.