Thinking about order: a review of common processing of magnitude and learned orders in animals.

Rich behavioral and neurobiological evidence suggests cognitive and neural overlap in how quantitatively comparable dimensions such as quantity, time, and space are processed in humans and animals. While magnitude domains such as physical magnitude, time, and space represent information that can be quantitatively compared (4 "is half of" 8), they also represent information that can be organized ordinally (1→2→3→4). Recent evidence suggests that the common representations seen across physical magnitude, time, and space domains in humans may be due to their common ordinal features rather than their common quantitative features, as these common representations appear to extend beyond magnitude domains to include learned orders. In this review, we bring together separate lines of research on multiple ordinal domains including magnitude-based and learned orders in animals to explore the extent to which there is support for a common cognitive process underlying ordinal processing. Animals show similarities in performance patterns across natural quantitatively comparable ordered domains (physical magnitude, time, space, dominance) and learned orders (acquired through transitive inference or simultaneous chaining). Additionally, they show transfer and interference across tasks within and between ordinal domains that support the theory of a common ordinal representation across domains. This review provides some support for the development of a unified theory of ordinality and suggests areas for future research to better characterize the extent to which there are commonalities in cognitive processing of ordinal information generally.

Does cognition differ across species, and how do we know? Lessons from research in transitive inference.

Comparative psychologists study cognition by characterizing the behavior of individual species and explicitly comparing behavior across species. We use the extensive comparative literature on transitive inference (TI) as a case study to evaluate four central methodological questions that continue to be debated in the field of comparative psychology: 1) Are contextual variables sufficient to explain species differences in cognition? 2) Can cognitive performance be accounted for by associative processes alone? 3) Can we determine the cognitive mechanisms by which animals solve tasks? and 4) What is the role of ecologically driven hypotheses in comparative psychology? Although contextual variables and associative processes undeniably influence choice behavior in TI tasks, neither is sufficient to explain all performance. Instead, multiple distinct cognitive mechanisms, including associative processes, logical inference, and spatial representations, can and do result in successful TI performance. TI is not a unitary task solved using a single mechanism; multiple processes are recruited, with their degree of involvement dependent on context, species, and evolutionary pressures. This suggests that rather than asking whether animals possess a certain cognitive ability, research should focus on differences in when and how species employ tools from what is often a reasonably similar cognitive toolbox. We join others who have proposed that a main goal of comparative psychology should be to determine how animals solve cognitive tasks, through minimizing and studying the influence of contextual variables, evaluating the contributions of associative processes, clearly characterizing and testing alternative cognitive mechanisms, and using strong evolutionary hypotheses to guide predictions. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Associative models fail to characterize transitive inference performance in rhesus monkeys (Macaca mulatta).

It has been suggested that non-verbal transitive inference (if A > B and B > C, then A > C) can be accounted for by associative models. However, little is known about the applicability of such models to primate data. In Experiment 1, we tested the fit of two associative models to primate data from both sequential training, in which the training pairs were presented in a backward order, and simultaneous training, in which all training pairs are presented intermixed from the beginning. We found that the models provided an equally poor fit for both sequential and simultaneous training presentations, contrary to the case with data from pigeons. The models were also unable to predict the robust symbolic distance effects characteristic of primate transitive choices. In Experiment 2, we used the models to fit a list-linking design in which two seven-item transitive lists were first trained independently (A > B…. > F > G and H > I …. > M > N) then combined via a linking pair (G+ H-) into a single, 14-item list. The model produced accurate predictions for between-list pairs, but did not predict transitive responses for within-list pairs from list 2. Overall, our results support research indicating that associative strength does not adequately account for the behavior of primates in transitive inference tasks. The results also suggest that transitive choices may result from different processes, or different weighting of multiple processes, across species.

Smaller on the left? Flexible association between space and magnitude in pigeons (Columba livia) and blue jays (Cyanocitta cristata).

Humans and other apes represent magnitudes spatially, demonstrated by their responding faster and more accurately to one side of space when presented with small quantities and to the other side of space when presented with large quantities. This representation is flexible and shows substantial variability between cultural groups in humans and between and within individuals in great apes. In contrast, recent findings suggest that chicks show a spatial representation of magnitude that is highly lateralized and inflexible, implying a qualitatively different underlying representation than in primates. Using methods similar to those used with great apes and humans, we trained adult domestic pigeons (Columba livia) and blue jays (Cyanocitta cristata) to select the smaller (or larger) of two nonadjacent quantity arrays; later, this task was reversed. At test, birds were presented with novel probe pairs consisting of adjacent quantity pairs (e.g., 2 vs. 3). Both species showed robust evidence for a flexible spatial representation of magnitude with considerable individual variability in the orientation of this representation. These results are not consistent with an inflexible, lateralized, left-to-right representation of magnitude in birds, but are consistent with the flexible spatial representation of magnitude observed in apes and humans. We conclude that the tendency to organize quantities spatially may be a fundamental and evolutionarily ancient feature of cognition that is widespread among vertebrates. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Red is the new orange: Nonlinguistic categorical color perception.

Caves et al. (2018) demonstrated categorical perception in zebra finches for the orange-red color category that conveys information about male fitness. This result implies that categorical color perception does not necessarily have linguistic origins, as has been previously believed.

Implicit relational learning in a multiple-object tracking task.

We studied implicit relational learning by embedding contextual relational information into a multiple-object tracking task. In two experiments, participants were instructed to track two or four out of eight moving objects and report at the end of the trial whether a single cued object was among those they tracked (yes/no task). The stimulus display also contained two background strips of different width. In the informative condition, the location of the cued object predicted the correct choice: If the answer was "yes", then the cued object was always located next to the narrower strip; otherwise, it was always located next to the wider strip (or vice versa). In the random condition, the location of the object did not predict the correct choice. Participants in the informative condition consistently displayed lower tracking accuracy than in the random condition, possibly due to attentional demands introduced by implicit relational task. At the same time, participants in the informative condition demonstrated no awareness of the task structure; instead, their reports were consistent with the attempts to track moving objects. Our task can provide a suitable model for studying implicit relational learning in adult participants that is essential for establishing generality of factors affecting relational learning.

Pharmacological manipulation of GABA activity in nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS) impairs figure-ground discrimination in pigeons: Running head: SP/IPS in figure-ground segregation.

Figure-ground segregation is a fundamental visual ability that allows an organism to separate an object from its background. Our earlier research has shown that nucleus rotundus (Rt), a thalamic nucleus processing visual information in pigeons, together with its inhibitory complex, nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS), are critically involved in figure-ground discrimination (Acerbo et al., 2012; Scully et al., 2014). Here, we further investigated the role of SP/IPS by conducting bilateral microinjections of GABAergic receptor antagonist and agonists (bicuculline and muscimol, respectively) and non-NMDA glutamate receptor antagonist (CNQX) after the pigeons mastered figure-ground discrimination task. We used two doses of each drug (bicuculline: 0.1 mM and 0.05 mM; muscimol: 4.4 mM and 8.8 mM; CNQX: 2.15 mM and 4.6 mM) in a within-subject design, and alternated drug injections with baseline (ACSF). The order of injections was randomized across birds to reduce potential carryover effects. We found that a low dose of bicuculline produced a decrement on figure trials but not on background trials, whereas a high dose impaired performance on background trials but not on figure trials. Muscimol produced an equivalent, dose-dependent impairment on both types of trials. Finally, CNQX had no consistent effect at either dose. Together, these results further confirm our earlier hypothesis that inhibitory projections from SP to Rt modulate figure-ground discrimination, and suggest that the Rt and the SP/IPS provide a plausible substrate that could perform figure-ground segregation in avian brain.

No evidence for feature binding by pigeons in a change detection task.

We trained pigeons to respond to one key when two consecutive displays were the same as one another (no-change trial) and to respond to another key when the two displays were different from one another (change trial; change detection task). Change-trial displays were distinguished by a change in all three features (color, orientation, and location) of all four items presented in the display. Pigeons learned this change-no change discrimination to high levels of accuracy. In Experiments 1 and 2, we compared replace trials in which one or two features were replaced by novel features to switch trials in which the features were exchanged among the objects. Pigeons reported both replace and switch trials as "no-change" trials. In contrast, adult humans in Experiment 3 reported both types of trials as "change" trials and showed robust evidence for feature binding. In Experiment 4, we manipulated the total number of objects in the display and the number of objects that underwent change. Unlike people, pigeons showed strong control by the number of feature changes in the second display; pigeons' failure to exhibit feature binding may therefore be attributed to their failure to attend to items in the displays as integral objects.

Hippocampal lesion and transitive inference: dissociation of inference-based and reinforcement-based strategies in pigeons.

A typical nonverbal transitive inference task (TI) consists of several overlapping discriminations (A+ B-, B+ C-, C+ D-, D+ E-, where letters indicate stimuli and pluses and minuses denote reinforcement and nonreinforcement). A choice of stimulus B in a novel pair BD is interpreted as indicative of a TI (if B > C and C > D, then B > D). Although hippocampus has been implicated in nonverbal TI, it is not clear whether it simply maintains memory of associative values or stores an ordered representation of stimuli. We investigated the effect of hippocampal lesion on TI in pigeons while controlling reinforcement history so that reliance on associative values would lead to a choice of a stimulus D in the pair BD instead of a choice of a stimulus B expected by inferential mechanisms. Prior to the lesion, some of the pigeons (relational group; n = 4) have selected B over D indicating TI, while other birds (associative group; n = 6) chose D over B suggesting reliance on associative values. Hippocampal lesion had no effect on postlesion performance in associative group. In contrast, the relational group that preferred stimulus B in a pair BD before lesion showed a near-chance performance after the lesion. Our results demonstrate that hippocampus may be involved in creating a representation of an ordered series of the stimuli instead of maintaining reinforcement history of each stimulus. In addition, we provide a behavioral procedure suitable for dissociating different behavioral strategies used to solving TI task. Finally, we show for the first time the involvement of avian hippocampus in the task that is not explicitly spatial in nature. These results further confirm the notion that avian hippocampus is functionally analogous to mammalian hippocampus despite the significant differences in their anatomy.

Effects of spatial training on transitive inference performance in humans and rhesus monkeys.

It is often suggested that transitive inference (TI; if A > B and B > C, then A > C) involves mentally representing overlapping pairs of stimuli in a spatial series. However, there is little direct evidence to unequivocally determine the role of spatial representation in TI. We tested whether humans and rhesus monkeys use spatial representations in TI by training them to organize 7 images in a vertical spatial array. Then, we presented subjects with a TI task using these same images. The implied TI order was either congruent or incongruent with the order of the trained spatial array. Humans in the congruent condition learned premise pairs more quickly, and were faster and more accurate in critical probe tests, suggesting that the spatial arrangement of images learned during spatial training influenced subsequent TI performance. Monkeys first trained in the congruent condition also showed higher test trial accuracy when the spatial and inferred orders were congruent. These results directly support the hypothesis that humans solve TI problems by spatial organization, and suggest that this cognitive mechanism for inference may have ancient evolutionary roots.

A three-component model of relational responding in the transposition paradigm.

We present a new model of transposition behavior that involves 3 predictors: (a) the disparity in generalized associative strength from the previously reinforced and nonreinforced stimuli (g) to the stimuli in the testing pair; (b) relational disparity (r), the difference in the logarithmically scaled sensory values of the testing stimuli; and (c) familiarity (f), the inverse of the Euclidean distance from the testing pair to the nearest training pair in 2-dimensional stimulus space. We evaluated the model with pigeons as subjects and with circle diameter (Experiment 1) and speed of motion (Experiment 2) as sensory dimensions. In each experiment, we presented 1, 2, or 3 training pairs as well as a wide range of testing pairs, including those comprising nonadjacent training stimuli. The control that was exerted by g did not depend on the number of training pairs and predicted behavior better than r and f after 1-pair training. In contrast, the influence of r increased dramatically with an increase in the number of training pairs. The contribution of f depended on the stimulus domain: When circle area was used (Experiment 1), the influence of f was similar to r; however, when speed of motion was used (Experiment 2), f had no discernible effect on pigeons' behavior. In sum, our results suggest that pigeons' transposition behavior is affected by both reinforcement history (g) and the relation between the experimental stimuli (r and f); our model provides a principled means for assessing the relative contribution of each predictor to choice behavior.

Bilateral lesions of nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS) selectively impair figure-ground discrimination in pigeons.

Earlier, we reported that nucleus rotundus (Rt) together with its inhibitory complex, nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS), had significantly higher activity in pigeons performing figure-ground discrimination than in the control group that did not perform any visual discriminations. In contrast, color discrimination produced significantly higher activity than control in the Rt but not in the SP/IPS. Finally, shape discrimination produced significantly lower activity than control in both the Rt and the SP/IPS. In this study, we trained pigeons to simultaneously perform three visual discriminations (figure-ground, color, and shape) using the same stimulus displays. When birds learned to perform all three tasks concurrently at high levels of accuracy, we conducted bilateral chemical lesions of the SP/IPS. After a period of recovery, the birds were retrained on the same tasks to evaluate the effect of lesions on maintenance of these discriminations. We found that the lesions of the SP/IPS had no effect on color or shape discrimination and that they significantly impaired figure-ground discrimination. Together with our earlier data, these results suggest that the nucleus Rt and the SP/IPS are the key structures involved in figure-ground discrimination. These results also imply that thalamic processing is critical for figure-ground segregation in avian brain.

Figure-ground discrimination in the avian brain: the nucleus rotundus and its inhibitory complex.

In primates, neurons sensitive to figure-ground status are located in striate cortex (area V1) and extrastriate cortex (area V2). Although much is known about the anatomical structure and connectivity of the avian visual pathway, the functional organization of the avian brain remains largely unexplored. To pinpoint the areas associated with figure-ground segregation in the avian brain, we used a radioactively labeled glucose analog to compare differences in glucose uptake after figure-ground, color, and shape discriminations. We also included a control group that received food on a variable-interval schedule, but was not required to learn a visual discrimination. Although the discrimination task depended on group assignment, the stimulus displays were identical for all three experimental groups, ensuring that all animals were exposed to the same visual input. Our analysis concentrated on the primary thalamic nucleus associated with visual processing, the nucleus rotundus (Rt), and two nuclei providing regulatory feedback, the pretectum (PT) and the nucleus subpretectalis/interstitio-pretecto-subpretectalis complex (SP/IPS). We found that figure-ground discrimination was associated with strong and nonlateralized activity of Rt and SP/IPS, whereas color discrimination produced strong and lateralized activation in Rt alone. Shape discrimination was associated with lower activity of Rt than in the control group. Taken together, our results suggest that figure-ground discrimination is associated with Rt and that SP/IPS may be a main source of inhibitory control. Thus, figure-ground segregation in the avian brain may occur earlier than in the primate brain.

Relational learning in a context of transposition: a review.

In a typical transposition task, an animal is presented with a single pair of stimuli (for example, S3+ S4-, where plus and minus denote reward and nonreward and digits denote stimulus location on a sensory dimension such as size). Subsequently, an animal is presented with a testing pair that contains a previously reinforced or nonreinforced stimulus and a novel stimulus (for example, S2-S3 and S4-S5). Does the choice of a novel S2 instead of previously reinforced S3 in a testing pair S2-S3 indicate that the animal has learned a relation (i.e., "select smaller")? This review of empirical evidence and theoretical accounts shows that an organism's behavior in a transposition task is undoubtedly influenced by prior reinforcement history of the training stimuli (Spence, 1937). However, it is also affected by two other factors that are relational in nature-a similarity of two testing stimuli to each other and an overall similarity of the testing pair as a whole to the training pair as a whole. The influence of the two latter factors is especially evident in studies that use multiple pairs of training stimuli and a wide range of testing pairs comprising nonadjacent stimuli (Lazareva, Miner, Young, & Wasserman, 2008; Lazareva, Wasserman, & Young, 2005). In sum, the evidence suggests that both prior reinforcement history and relational information affect an animal's behavior in a typical transposition task.

Transitive inference in pigeons: measuring the associative values of Stimuli B and D.

Several reinforcement-based models have been proposed to explain transitive-like behavior in nonverbal transitive inference tasks. These models assume that the initial training required for memorizing the premises produces an ordered series of associative values (A>B>C>D>E); these values can then be used to select the "transitively correct" stimulus in a novel pair (e.g., BD). Our study experimentally tested this assumption by using resistance-to-extinction and resistance-to-reinforcement techniques to obtain empirical measures of associative strength for Stimuli B and D. We first measured the associative strengths of these stimuli after completion of initial training with overlapping pairs of colored squares (A+B-, B+C-, C+D-, and D+E-) using resistance-to-extinction and resistance-to-reinforcement procedures. Next, we used massed presentations of Pair D+E- (termed bias reversal) that ought to increase the associative value of Stimulus D, and again measured the associative strengths of the stimuli. None of our experimental measures of associative strength correlated with pigeons' behavior in the BD test or with BD performance predicted by associative models either before or after bias reversal (Wynne, 1995; Siemann and Delius, 1998). These results question validity of reinforcement-based models for explaining animals' behavior in nonverbal TI tasks.

Effect of between-category similarity on basic level superiority in pigeons.

Children categorize stimuli at the basic level faster than at the superordinate level. We hypothesized that between-category similarity may affect this basic level superiority effect. Dissimilar categories may be easy to distinguish at the basic level but be difficult to group at the superordinate level, whereas similar categories may be easy to group at the superordinate level but be difficult to distinguish at the basic level. Consequently, similar basic level categories may produce a superordinate-before-basic learning trend, whereas dissimilar basic level categories may result in a basic-before-superordinate learning trend. We tested this hypothesis in pigeons by constructing superordinate level categories out of basic level categories with known similarity. In Experiment 1, we experimentally evaluated the between-category similarity of four basic level photographic categories using multiple fixed interval-extinction training (Astley and Wasserman, 1992). We used the resultant similarity matrices in Experiment 2 to construct two superordinate level categories from basic level categories with high between-category similarity (cars and persons; chairs and flowers). We then trained pigeons to concurrently classify those photographs into either the proper basic level category or the proper superordinate level category. Under these conditions, the pigeons learned the superordinate level discrimination faster than the basic level discrimination, confirming our hypothesis that basic level superiority is affected by between-category similarity.

Changes in area affect figure-ground assignment in pigeons.

A critical cue for figure-ground assignment in humans is area: smaller regions are more likely to be perceived as figures than are larger regions. To see if pigeons are similarly sensitive to this cue, we trained birds to report whether a target appeared on a colored figure or on a differently colored background. The initial training figure was either smaller than (Experiments 1 and 2) or the same area as (Experiment 2) the background. After training, we increased or decreased the size of the figure. When the original training shape was smaller than the background, pigeons' performance improved with smaller figures (and worsened with larger figures); when the original training shape was the same area as the background, pigeons' performance worsened when they were tested with smaller figures. A smaller figural region appeared to improve the figure-ground discrimination only when size was a relevant cue in the initial discrimination.

Nonverbal transitive inference: Effects of task and awareness on human performance.

We studied human nonverbal transitive inference in two paradigms: with choice stimuli orderable along a physical dimension and with non-orderable choice stimuli. We taught 96 participants to discriminate four overlapping pairs of choice stimuli: A+ B-, B+ C-, C+ D-, and D+ E-. Half of the participants were provided with post-choice visual feedback stimuli which were orderable by size; the other half were not provided with orderable feedback stimuli. In later testing, we presented novel choice pairs: BD, AC, AD, AE, BE, and CE. We found that transitive responding depended on task awareness for all participants. Additionally, participants given ordered feedback showed clearer task awareness and stronger transitive responding than did participants not given ordered feedback. Associative models (Wynne, 1995; Siemann and Delius, 1998) failed to predict the increase in transitive responding with increasing awareness. These results suggest that ordered and non-ordered transitive inference tasks support different patterns of performance.

Effects of stimulus duration and choice delay on visual categorization in pigeons.

We (Lazareva, Freiburger, & Wasserman, 2004) previously trained four pigeons to classify color photographs into their basic-level categories (cars, chairs, flowers, or people) or into their superordinate-level categories (natural or artificial). Here, we found that brief stimulus durations had the most detrimental effect on the basic-level discrimination of natural stimuli by the same pigeons. Increasing the delay between stimulus presentation and choice responding had greater detrimental effect on the basic-level discrimination than the superordinate-level discrimination. These results suggest that basic-level discriminations required longer stimulus durations and were more subject to forgetting than were superordinate-level discriminations. Additionally, categorization of natural stimuli required longer stimulus durations than categorization of artificial stimuli, but only at the basic level. Together, these findings suggest that basic-level categorization may not always be superior to superordinate-level categorization and provide additional evidence of a dissociation between natural and artificial stimuli in pigeons' categorization.