Beyond the mark: Signatures of self-recognition in fish.

A new study with cleaner fish demonstrates the need to expand cognitive testing of animals beyond success testing (a simple pass or fail criteria), and instead investigate the signatures of how animals solve tasks. By tailoring traditional cognitive tests to the focal species' natural behaviour, researchers can provide animals with a better chance for demonstrating their cognitive abilities, offering a more comprehensive understanding of the evolution of cognition.

The effects of hippocampal and area parahippocampalis lesions on the processing and retention of serial-order behavior, autoshaping, and spatial behavior in pigeons.

We examined the role of the avian hippocampus and area parahippocampalis in serial-order behavior and a variety of other tasks known to be sensitive to hippocampal damage in mammals. Damage to the hippocampus and area parahippocampalis caused impairments in autoshaping and performance on an analogue of a radial-arm maze task, but had no effect on acquisition of 2-item, 3-item, and 4-item serial-order lists. Additionally, the lesions had no effect on the retention of 3-items lists, or on the ability to perform novel derived lists composed of elements from lists they had previously learned. The impairments in autoshaping and spatial behavior are consistent with the findings in mammals. The absence of impairments on the serial-order task may also be consistent once one considers that damage to the hippocampus in mammals seems to affect more internally-organized rather than externally-organized serial-order tasks. Together, the findings support the view that the avian hippocampal complex serves a function very similar to the mammalian hippocampus, a finding that is interesting given that the architecture of the avian hippocampus differs dramatically from that of the mammalian hippocampus.

Delay activity in the Wulst of pigeons (Columba livia) represents correlates of both sample and reward information.

The avian Wulst is the pallial (analogous to mammalian cortex) termination point of the thalamofugal pathway, one of two main visual pathways in birds, and is considered to be equivalent to primate striate cortex. We recorded neuronal activity from the Wulst in pigeons during two versions of a delayed matching-to-sample procedure. Two birds were trained on a common outcomes (CO) procedure, in which correct responses following both the skateboarder and the flower stimuli were associated with reward. Two other birds were trained on a differential outcomes (DO) procedure in which correct responses following only the skateboarder stimulus were associated with reward, while correct responses following the flower stimulus were not rewarded. In line with previous studies, under CO conditions, and for both excitatory and inhibitory neurons, delay activity in the Wulst was significantly different from baseline activity following both sample stimuli, which may indicate that Wulst delay activity is a neural correlate of working memory for the sample stimulus. On the other hand, under DO conditions, Wulst delay activity appeared to be a neural correlate of the upcoming reward. We argue that Wulst neurons display flexibility in their encoding in that they can encode both sample and reward information, but may default to one type of coding over the other based on the demands of the task. The current study provides the first evidence that delay activity in the Wulst represents both a neural correlate for sample information as well as reward information.

Orthographic processing in pigeons (Columba livia).

Learning to read involves the acquisition of letter-sound relationships (i.e., decoding skills) and the ability to visually recognize words (i.e., orthographic knowledge). Although decoding skills are clearly human-unique, given they are seated in language, recent research and theory suggest that orthographic processing may derive from the exaptation or recycling of visual circuits that evolved to recognize everyday objects and shapes in our natural environment. An open question is whether orthographic processing is limited to visual circuits that are similar to our own or a product of plasticity common to many vertebrate visual systems. Here we show that pigeons, organisms that separated from humans more than 300 million y ago, process words orthographically. Specifically, we demonstrate that pigeons trained to discriminate words from nonwords picked up on the orthographic properties that define words and used this knowledge to identify words they had never seen before. In addition, the pigeons were sensitive to the bigram frequencies of words (i.e., the common co-occurrence of certain letter pairs), the edit distance between nonwords and words, and the internal structure of words. Our findings demonstrate that visual systems organizationally distinct from the primate visual system can also be exapted or recycled to process the visual word form.

Effects of nidopallium caudolaterale inactivation on serial-order behavior in pigeons ( Columba livia).

Serial-order behavior is the ability to complete a sequence of responses in a predetermined order to achieve a reward. In birds, serial-order behavior is thought to be impaired by damage to the nidopallium caudolaterale (NCL). In the current study, we examined the role of the NCL in serial-order behavior by training pigeons on a 4-item serial-order task and a go/no-go discrimination task. Following training, pigeons received infusions of 1 µl of either tetrodotoxin (TTX) or saline. Saline infusions had no impact on serial-order behavior, whereas TTX infusions resulted in a significant decrease in performance. The serial-order impairments, however, were not the result of any specific error at any specific list item. With respect to the go/no-go discrimination task, saline infusions also had no impact on performance, whereas TTX infusions impaired pigeons' discrimination abilities. Given the impairments on the go/no-go discrimination task, which does not require processing of serial-order information, we tentatively conclude that damage to the NCL does not impair serial-order behavior per se, but rather results in a more generalized impairment that may impact performance across a range of tasks. NEW & NOTEWORTHY We examined the role of the nidopallium caudolaterale (NCL) in serial-order behavior by training pigeons on a 4-item serial-order task and selectively inhibiting the region with TTX. Although TTX infusions did impair serial-order behavior, the pattern of the deficit, plus the fact that TTX also impaired performance on a task without a serial-order component, indicates that inactivation of NCL causes impairments in reward processing or inhibition rather than serial-order behavior.

Do 'literate' pigeons (Columba livia) show mirror-word generalization?

Many children pass through a mirror stage in reading, where they write individual letters or digits in mirror and find it difficult to correctly utilize letters that are mirror images of one another (e.g., b and d). This phenomenon is thought to reflect the fact that the brain does not naturally discriminate left from right. Indeed, it has been argued that reading acquisition involves the inhibition of this default process. In the current study, we tested the ability of literate pigeons, which had learned to discriminate between 30 and 62 words from 7832 nonwords, to discriminate between words and their mirror counterparts. Subjects were sensitive to the left-right orientation of the individual letters, but not the order of letters within a word. This finding may reflect the fact that, in the absence of human-unique top-down processes, the inhibition of mirror generalization may be limited.

Visual response properties of neurons in four areas of the avian pallium.

In the present study we investigate the visual responsiveness of neurons in the entopallium, arcopallium, nidopallium, and hippocampus of pigeons. Pigeons were presented with 12 different stimuli, including three stimuli of a pigeon (a portrait of a pigeon's face, a profile view of a pigeon's face, and a picture of a whole pigeon). A total of 53 cells were recorded from the entopallium, 65 from the arcopallium, 32 from the nidopallium, and 67 from the hippocampus. Although a number of neurons were selective for certain colours and shapes, no neurons were solely selective for the three pigeon stimuli. This finding contrasts with previous studies across a range of mammals demonstrating selective firing to images of conspecifics. Rather than reflecting an absence of these cells in pigeons, we argue our findings may reflect the difficulty pigeons have in understanding the correspondence between 2D representations of 3D stimuli.

To have and to hold: episodic memory in 3- and 4-year-old children.

Episodic memory endows us with the ability to reflect on our past and plan for our future. Most theorists argue that episodic memory emerges during the preschool period and that its emergence might herald the end of childhood amnesia. Here, we show that both 3- and 4-year-old children form episodic memories, but that 3-year-old children fail to retain those memories following a delay (Experiments 1 and 2). In contrast, 4-year-old children retained episodic memories over delays of 24 hr (Experiment 1) and 1 week (Experiment 3). This marked change in the retention of episodic memories between 3 and 4 years of age suggests that it is our ability to retain, rather than to form, an episodic memory that limits our ability to recall episodes from early childhood.

Seeing the Forest for the Trees, and the Ground Below My Beak: Global and Local Processing in the Pigeon's Visual System.

Non-human animals tend to solve behavioral tasks using local information. Pigeons are particularly biased toward using the local features of stimuli to guide behavior in small-scale environments. When behavioral tasks are performed in large-scale environments, pigeons are much better global processors of information. The local and global strategies are mediated by two different fovea in the pigeon retina that are associated with the tectofugal and thalamofugal pathways. We discuss the neural mechanisms of pigeons' bias for local information within the tectofugal pathway, which terminates at an intermediate stage of extracting shape complexity. We also review the evidence suggesting that the thalamofugal pathway participates in global processing in pigeons and is primarily engaged in constructing a spatial representation of the environment in conjunction with the hippocampus.

The effect of progressive image scrambling on neuronal responses at three stations of the pigeon tectofugal pathway.

The progressive image scrambling procedure is an effective way of determining sensitivity to image features at different stages of the visual system, but it hasn't yet been used to evaluate neuronal responses in birds. We determined the effect of progressively scrambling images of objects on the population responses of anterior entopallium (ENTO), mesopallium ventrolaterale (MVL), and posterior nidopallium intermediate pars lateralis (NIL) in pigeons. We found that MVL responses were more sensitive to both the intact objects and the highly scrambled images, whereas ENTO showed no clear preference for the different stimuli. In contrast, the NIL population response strongly preferred the original images over the scrambled images. These findings suggest that the anterior tectofugal pathway may process local shape in a hierarchical manner, and the posterior tectofugal pathway may process global shape of greater complexity. Another possibility is that the differential responses between ENTO/MVL and NIL may reflect an anterior-posterior map of varying sensitivity to spatial frequency.

Neurons in the pigeon visual network discriminate between faces, scrambled faces, and sine grating images.

Discriminating between object categories (e.g., conspecifics, food, potential predators) is a critical function of the primate and bird visual systems. We examined whether a similar hierarchical organization in the ventral stream that operates for processing faces in monkeys also exists in the avian visual system. We performed electrophysiological recordings from the pigeon Wulst of the thalamofugal pathway, in addition to the entopallium (ENTO) and mesopallium ventrolaterale (MVL) of the tectofugal pathway, while pigeons viewed images of faces, scrambled controls, and sine gratings. A greater proportion of MVL neurons fired to the stimuli, and linear discriminant analysis revealed that the population response of MVL neurons distinguished between the stimuli with greater capacity than ENTO and Wulst neurons. While MVL neurons displayed the greatest response selectivity, in contrast to the primate system no neurons were strongly face-selective and some responded best to the scrambled images. These findings suggest that MVL is primarily involved in processing the local features of images, much like the early visual cortex.

Delay activity in avian prefrontal cortex--sample code or reward code?

In the current study, we examined whether delay activity in the avian equivalent of the prefrontal cortex (PFC) represents a neural correlate of a to-be-remembered sample stimulus or an upcoming reward. Birds were trained on a directed forgetting paradigm in which sample stimuli (red and white) were either followed by a cue to remember (high-frequency tone) or a cue to forget (low-frequency tone). The task also incorporated a differential outcomes procedure in which a correct response on the memory test following a red (remember) sample was rewarded with food, but correct responses on the memory test following the white (remember) sample were not. If delay activity represents a sample code, then it should be seen on both red-remember and white-remember trials. On the other hand, if delay activity represents a reward code, then delay activity should be seen only on red-remember trials, but not white-remember trials. Our findings suggest that activity in the avian PFC represents the outcome associated with each sample (reward or no reward) rather than memory for the sample itself.

Sequential planning in rhesus monkeys (Macaca mulatta).

In the current study, we examined the planning abilities of rhesus monkeys (Macaca mulatta) by training them on a five-item list composed of coloured photographs and then testing them on switch and mask trials. In contrast to previous studies where monkeys made responses using a joystick, in the current study, monkeys made responses directly to a touch screen. On switch trials, after a response to the first list item, the on-screen positions of two list items were exchanged. Performance on trials in which the second and third list items were exchanged was poorer compared to normal (non-switch) trials for all subjects. When the third and fourth items were exchanged, however, only one subject continued to show performance deficits. On mask trials, following a response to the first item, the remaining items were covered by opaque white squares. When two items were masked, all four subjects responded to each masked item at a level significantly above chance. When three items were masked, however, only one subjected was able to respond to all three masked items at a level significantly above chance. The results of the present study indicate that three of our four monkeys planned one response ahead while a single monkey planned two responses ahead. The significance of these findings is discussed in relation to previous studies on planning in chimpanzees and monkeys.

A positional coding mechanism in pigeons after learning multiple three-item lists.

Pigeons were trained on three three-item lists (List 1: A(1) --> B(1) --> C(1;) List 2: A(2) --> B(2) --> C(2;) List 3: A(3) --> B(3) --> C(3)). After sessions in which any one of the three lists could be presented on a trial, derived-maintained list and derived-changed list probe trials were introduced. The derived list probe trials were composed of three items, one drawn from each of the training lists. On derived-maintained probe trials, each item was in the same ordinal position it occupied during training (e.g., A(3) --> B(1) --> C(2)). On derived-changed probe trials, items that occupied the second and third position during training were exchanged (e.g., A(2) --> C(3) --> B(1)). The performance of subjects on derived-maintained probe trials was significantly above chance and no different to that observed on the training lists. In contrast, subjects' performance on derived-changed probe trials was significantly below chance. To our knowledge, this is the first study that has demonstrated pigeons are able to learn and retain multiple three-item lists. In addition, subjects' performance on the derived-maintained probe trials suggests that they acquire knowledge of each list item's ordinal position when learning multiple lists.

Are There Differences in "Intelligence" Between Nonhuman Species? The Role of Contextual Variables.

We review evidence for Macphail's (1982, 1985, 1987) Null Hypothesis, that nonhumans animals do not differ either qualitatively or quantitatively in their cognitive capacities. Our review supports the Null Hypothesis in so much as there are no qualitative differences among nonhuman vertebrate animals, and any observed differences along the qualitative dimension can be attributed to failures to account for contextual variables. We argue species do differ quantitatively, however, and that the main difference in "intelligence" among animals lies in the degree to which one must account for contextual variables.

The functional architecture, receptive field characteristics, and representation of objects in the visual network of the pigeon brain.

We provide an extensive review of the pigeon visual system, focussing on the known cell types, receptive field characteristics, mechanisms of perception/visual attention, and projection profiles of neurons in the thalamofugal and tectofugal pathways. The similarities and differences with the primate visual system at each stage of the visual hierarchy are highlighted. We conclude with a discussion of object and face processing in birds, as well as the current state of knowledge in the search for face-selective neurons in the avian visual system.

Nidopallium caudolaterale neuronal responses during serial-order behaviour in pigeons.

Serial-order behaviour is the ability to complete a sequence of responses in order to obtain a reward. Serial-order tasks can be thought of as either externally-ordered (EO) such that the order of responses is predetermined, or internally-ordered (IO) such that the subject determines the order of responses from trial to trial. Ordinal knowledge (representation of first, second, or third etc.) is a key component of successful serial-order behaviour, and is considered a higher-order cognitive function. The nidopallium caudolaterale (NCL) is the avian equivalent to the prefrontal cortex, an area of the primate brain important for serial-order behaviour. The importance of the NCL for serial-order behaviour, however, is still unknown. In the current study, we trained pigeons to complete either three-item EO or IO tasks and recorded single-neuron activity from the NCL to determine whether neurons in the NCL code ordinal knowledge. Our results support the view that the NCL is involved in serial-order behaviour by coding ordinal position, at least with respect to the IO task. The absence of any ordinal coding during the EO task could be explained by the different strategies that birds adopt between the EO and IO tasks.

Pigeon nidopallium caudolaterale, entopallium, and mesopallium ventrolaterale neural responses during categorisation of Monet and Picasso paintings.

Pigeons can successfully discriminate between sets of Picasso and Monet paintings. We recorded from three pallial brain areas: the nidopallium caudolaterale (NCL), an analogue of mammalian prefrontal cortex; the entopallium (ENTO), an intermediary visual area similar to primate extrastriate cortex; and the mesopallium ventrolaterale (MVL), a higher-order visual area similar to primate higher-order extrastriate cortex, while pigeons performed an S+/S- Picasso versus Monet discrimination task. In NCL, we found that activity reflected reward-driven categorisation, with a strong left-hemisphere dominance. In ENTO, we found that activity reflected stimulus-driven categorisation, also with a strong left-hemisphere dominance. Finally, in MVL, we found that activity reflected stimulus-driven categorisation, but no hemispheric differences were apparent. We argue that while NCL and ENTO primarily use reward and stimulus information, respectively, to discriminate Picasso and Monet paintings, both areas are also capable of integrating the other type of information during categorisation. We also argue that MVL functions similarly to ENTO in that it uses stimulus information to discriminate paintings, although not in an identical way. The current study adds some preliminary evidence to previous literature which emphasises visual lateralisation during discrimination learning in pigeons.

Avian Brains: Primate-like Functions of Neurons in the Crow Brain.

Despite the negative connotations of the term 'birdbrain', birds possess cognitive abilities on par with primates. A new study finds that neurons in the crow's brain display characteristics similar to those displayed by neurons in the primate's brain.