The neuroscience of perceptual categorization in pigeons: A mechanistic hypothesis.

We are surrounded by an endless variation of objects. The ability to categorize these objects represents a core cognitive competence of humans and possibly all vertebrates. Research on category learning in nonhuman animals started with the seminal studies of Richard Herrnstein on the category "human" in pigeons. Since then, we have learned that pigeons are able to categorize a large number of stimulus sets, ranging from Cubist paintings to English orthography. Strangely, this prolific field has largely neglected to also study the avian neurobiology of categorization. Here, we present a hypothesis that combines experimental results and theories from categorization research in pigeons with neurobiological insights on visual processing and dopamine-mediated learning in primates. We conclude that in both fields, similar conclusions on the mechanisms of perceptual categorization have been drawn, despite very little cross-reference or communication between these two areas to date. We hypothesize that perceptual categorization is a two-component process in which stimulus features are first rapidly extracted in a feed-forward process, thereby enabling a fast subdivision along multiple category borders. In primates this seems to happen in the inferotemporal cortex, while pigeons may primarily use a cluster of associative visual forebrain areas. The second process rests on dopaminergic error-prediction learning that enables prefrontal areas to connect top down the relevant visual category dimension to the appropriate action dimension.

Sneaking a peek: pigeons use peripheral vision (not mirrors) to find hidden food.

A small number of species are capable of recognizing themselves in the mirror when tested with the mark-and-mirror test. This ability is often seen as evidence of self-recognition and possibly even self-awareness. Strangely, a number of species, for example monkeys, pigs and dogs, are unable to pass the mark test but can locate rewarding objects by using the reflective properties of a mirror. Thus, these species seem to understand how a visual reflection functions but cannot apply it to their own image. We tested this discrepancy in pigeons-a species that does not spontaneously pass the mark test. Indeed, we discovered that pigeons can successfully find a hidden food reward using only the reflection, suggesting that pigeons can also use and potentially understand the reflective properties of mirrors, even in the absence of self-recognition. However, tested under monocular conditions, the pigeons approached and attempted to walk through the mirror rather than approach the physical food, displaying similar behavior to patients with mirror agnosia. These findings clearly show that pigeons do not use the reflection of mirrors to locate reward, but actually see the food peripherally with their near-panoramic vision. A re-evaluation of our current understanding of mirror-mediated behavior might be necessary-especially taking more fully into account species differences in visual field. This study suggests that use of reflections in a mirrored surface as a tool may be less widespread than currently thought.

Adjusting foraging strategies: a comparison of rural and urban common mynas (Acridotheres tristis).

Establishment in urbanized environments is associated with changes in physiology, behaviour, and problem-solving. We compared the speed of learning in urban and rural female common mynas, Acridotheres tristis, using a standard visual discrimination task followed by a reversal learning phase. We also examined how quickly each bird progressed through different stages of learning, including sampling and acquisition within both initial and reversal learning, and persistence following reversal. Based on their reliance on very different food resources, we expected urban mynas to learn and reversal learn more quickly but to sample new contingencies for proportionately longer before learning them. When quantified from first presentation to criterion achievement, urban mynas took more 20-trial blocks to learn the initial discrimination, as well as the reversed contingency, than rural mynas. More detailed analyses at the level of stage revealed that this was because urban mynas explored the novel cue-outcome contingencies for longer, and despite transitioning faster through subsequent acquisition, remained overall slower than rural females. Our findings draw attention to fine adjustments in learning strategies in response to urbanization and caution against interpreting the speed to learn a task as a reflection of cognitive ability.

The 5-HT1A/1B-receptor agonist eltoprazine increases both catecholamine release in the prefrontal cortex and dopamine release in the nucleus accumbens and decreases motivation for reward and "waiting" impulsivity, but increases "stopping" impulsivity.

The 5-HT1A/1B-receptor agonist eltoprazine has a behavioral drug signature that resembles that of a variety of psychostimulant drugs, despite the differences in receptor binding profile. These psychostimulants are effective in treating impulsivity disorders, most likely because they increase norepinephrine (NE) and dopamine (DA) levels in the prefrontal cortex. Both amphetamine and methylphenidate, however, also increase dopamine levels in the nucleus accumbens (NAc), which has a significant role in motivation, pleasure, and reward. How eltoprazine affects monoamine release in the medial prefrontal cortex (mPFC), the orbitofrontal cortex (OFC), and the NAc is unknown. It is also unknown whether eltoprazine affects different forms of impulsivity and brain reward mechanisms. Therefore, in the present study, we investigate the effects of eltoprazine in rats in the following sequence: 1) the activity of the monoaminergic systems using in vivo microdialysis, 2) motivation for reward measured using the intracranial self-stimulation (ICSS) procedure, and finally, 3) "waiting" impulsivity in the delay-aversion task, and the "stopping" impulsivity in the stop-signal task. The microdialysis studies clearly showed that eltoprazine increased DA and NE release in both the mPFC and OFC, but only increased DA concentration in the NAc. In contrast, eltoprazine decreased 5-HT release in the mPFC and NAc (undetectable in the OFC). Remarkably, eltoprazine decreased impulsive choice, but increased impulsive action. Furthermore, brain stimulation was less rewarding following eltoprazine treatment. These results further support the long-standing hypothesis that "waiting" and "stopping" impulsivity are regulated by distinct neural circuits, because 5-HT1A/1B-receptor activation decreases impulsive choice, but increases impulsive action.

Reasoning about "Capability": Wild Robins Respond to Limb Visibility in Humans.

Little comparative work has focused on what nonhumans understand about what physical acts others are capable of performing, and none has yet done so in the wild, or within a competitive framework. This study shows that North Island robins visually attend to human limbs in the context of determining who to steal food from. We presented 24 wild North Island Robins (Petroica longipes) with two experimenters. Robins could choose to steal a mealworm from one of two experimenters: one whose limbs were exposed and one who underwent a range of visual obstructions in two experiments. In most conditions, robins preferred to steal food located near the experimenter whose limbs were obscured by a cloth or board rather than food located near the experimenter whose limbs were not obscured. The robins' responses indicate that human limb visibility is associated with reduced access to food. Current findings lay the groundwork for a closer look at the potential general use of causal reasoning in an inter-specific context of using limbs to perform physical acts, specifically within the context of pilfering. This study presents one of the first tests of the role of visual attendance of potential limb availability in a competitive context, and could provide an alternative hypothesis for how other species have passed tests designed to examine what individuals understand about the physical acts others are capable of performing.

Addition and subtraction in wild New Zealand robins.

This experiment aimed to investigate proto-arithmetic ability in a wild population of New Zealand robins. We investigated numerical competence from the context of computation: behavioural responses to arithmetic operations over small numbers of prey objects (mealworms). Robins' behavioural responses (such as search time) to the simple addition and subtraction problems presented in a Violation of Expectancy (VoE) paradigm were measured. Either a congruent (expected) or incongruent (unexpected) quantity of food items were hidden in a trap door out of view of the subject. Within view of the subject, a quantity of items were added into (and in some cases subtracted from) the apparatus which was either the same as that hidden, or different. Robins were then allowed them to find a quantity that either preserved or violated addition and subtraction outcomes. Robins searched around the apparatus longer when presented with an incongruent scenario violating arithmetic rules, demonstrating potential proto-arithmetic awareness of changes in prey quantity. This article is part of a Special Issue entitled: Cognition in the wild.

Relative quantity judgments between discrete spatial arrays by chimpanzees (Pan troglodytes) and New Zealand robins (Petroica longipes).

Quantity discrimination for items spread across spatial arrays was investigated in chimpanzees (Pan troglodytes) and North Island New Zealand robins (Petroica longipes), with the aim of examining the role of spatial separation on the ability of these 2 species to sum and compare nonvisible quantities which are both temporally and spatially separated, and to assess the likely mechanism supporting such summation performance. Birds and chimpanzees compared 2 sets of discrete quantities of items that differed in number. Six quantity comparisons were presented to both species: 1v2, 1v3, 1v5, 2v3, 2v4, and 2v5. Each was distributed 1 at a time across 2 7-location arrays. Every individual item was viewed 1 at a time and hidden, with no more than a single item in each location of an array, in contrast to a format where all items were placed together into 2 single locations. Subjects responded by selecting 1 of the 2 arrays and received the entire quantity of food items hidden within that array. Both species performed better than chance levels. The ratio of items between sets was a significant predictor of performance in the chimpanzees, but it was not significant for robins. Instead, the absolute value of the smaller quantity of items presented was the significant factor in robin responses. These results suggest a species difference for this task when considering various dimensions such as ratio or total number of items in quantity comparisons distributed across discrete 7-location arrays.

Wild robins (Petroica longipes) respond to human gaze.

Gaze following and awareness of attentional cues are hallmarks of human and non-human social intelligence. Here, we show that the North Island robin (Petroica longipes), a food-hoarding songbird endemic to New Zealand, responds to human eyes. Robins were presented with six different conditions, in which two human experimenters altered the orientation or visibility of their body, head or eyes in relation to mealworm prey. One experimenter had visual access to the prey, and the second experimenter did not. Robins were then given the opportunity to 'steal' one of two mealworms presented by each experimenter. Robins responded by preferentially choosing the mealworm in front of the experimenter who could not see, in all conditions but one. Robins failed to discriminate between experimenters who were facing the mealworm and those who had their head turned 90° to the side. This may suggest that robins do not make decisions using the same eye visibility cues that primates and corvids evince, whether for ecological, experiential or evolutionary reasons.

What counts for 'counting'? Chimpanzees, Pan troglodytes, respond appropriately to relevant and irrelevant information in a quantity judgment task.

Nonhuman animals quantify all manner of things, and the way in which this is done is fairly well understood. However, little research has been conducted to determine how they know what is or is not relevant in the instances in which they quantify stimuli. We assessed how four chimpanzees chose between two sets of food items when the items were distributed across separate spatial arrays. Each item was covered by a container, and then was revealed in sequence so that neither whole set was visible at one time. After all containers were revealed, some were revealed again. The chimpanzees should have ignored items that were seen a second time and instead enumerated each item only once. In another test, some of the items were transposed in location and then uncovered again. Here, the chimpanzees needed to recognize that the newly shown food items were ones they already had seen. Overall, the chimpanzees were successful in selecting the truly larger array of items despite these potential distracting re-presentations of items. Discrimination performance also reflected analogue magnitude estimation because comparisons of sets that differed by larger amounts were easier than comparisons that differed by smaller amounts. Thus, chimpanzee quantity judgments for nonvisible sets of items are inexact, but they include an aspect of control for determining when items are uniquely presented versus re-presented.

Large quantity discrimination by North Island robins (Petroica longipes).

While numerosity-representation and enumeration of different numbers of objects-and quantity discrimination in particular have been studied in a wide range of species, very little is known about the numerical abilities of animals in the wild. This study examined spontaneous relative quantity judgments (RQJs) by wild North Island robins (Petroica longipes) of New Zealand. In Experiment 1, robins were tested on a range of numerical values of up to 14 versus 16 items, which were sequentially presented and hidden. In Experiment 2, the same numerical contrasts were tested on a different group of subjects but quantities were presented as whole visible sets. Experiment 3 involved whole visible sets that comprised of exceedingly large quantities of up to 56 versus 64 items. While robins shared with other species a ratio-based representation system for representing very large values, they also appeared to have developed an object indexing system with an extended upper limit (well beyond 4) that may be an evolutionary response to ecological challenges faced by scatter-hoarding birds. These results suggest that cognitive mechanism influencing an understanding of physical quantity may be deployed more flexibly in some contexts than previously thought, and are discussed in light of findings across other mammalian and avian species.

Memory for multiple cache locations and prey quantities in a food-hoarding songbird.

Most animals can discriminate between pairs of numbers that are each less than four without training. However, North Island robins (Petroica longipes), a food-hoarding songbird endemic to New Zealand, can discriminate between quantities of items as high as eight without training. Here we investigate whether robins are capable of other complex quantity discrimination tasks. We test whether their ability to discriminate between small quantities declines with (1) the number of cache sites containing prey rewards and (2) the length of time separating cache creation and retrieval (retention interval). Results showed that subjects generally performed above-chance expectations. They were equally able to discriminate between different combinations of prey quantities that were hidden from view in 2, 3, and 4 cache sites from between 1, 10, and 60 s. Overall results indicate that North Island robins can process complex quantity information involving more than two discrete quantities of items for up to 1 min long retention intervals without training.