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 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.

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.

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.

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.

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.

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.

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.

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.

Neurons in the pigeon nidopallium caudolaterale, but not the corticoidea dorsolateralis, display value and effort discounting activity.

We recorded from single neurons in two areas of the pigeon brain while birds were required to peck a stimulus indicating either a high effort task or a low effort task would follow. Upon completion of the task the birds received the same reward. We found that activity in the nidopallium caudolaterale, an area equivalent to the mammalian prefrontal cortex, was modulated by the value of the reward that would be received based on how much effort was required to obtain it. Value coding was most prominent during the presentation of the stimulus indicating a high or low effort task, and in the delay period immediately prior to carrying out the effort task. In contrast, activity in the corticoidea dorsolateralis was not modulated by value, however, population firing patterns suggest that it may be involved in associating actions with outcomes. Our findings support the view that activity in the nidopallium caudolaterale reflects value of reward as a function of effort discounting and as such may serve functions similar to the mammalian anterior cingulate cortex.

Delay activity in pigeon nidopallium caudolaterale during a variable-delay memory task.

Neurons in the pigeon nidopallium caudolaterale (NCL) are important for the maintenance of information across delays as long as 3 s. In the current study, we recorded neural activity from the avian NCL of 3 birds trained on a working memory task with three different delay lengths intermixed within a session. We found that when the birds are unable to predict the upcoming delay length there is no evidence that NCL cells engage in temporal coding. Furthermore, delay activity did not differ between correct and incorrect trials. Both findings have implications for the function of delay activity and its role in supporting working memory. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

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.

Aniracetam does not improve working memory in neurologically healthy pigeons.

Understanding the effects of cognitive enhancing drugs is an important area of research. Much of the research, however, has focused on restoring memory following some sort of disruption to the brain, such as damage or injections of scopolamine. Aniracetam is a positive AMPA-receptor modulator that has shown promise for improving memory under conditions when the brain has been damaged, but its effectiveness in improving memory in neurologically healthy subjects is unclear. The aim of the present study was to examine the effects of aniracetam (100mg/kg and 200 mg/kg) on short-term memory in "neurologically healthy" pigeons. Pigeons were administered aniracetam via either intramuscular injection or orally, either 30 or 60 minutes prior to testing on a delayed matching-to-sample task. Aniracetam had no effect on the pigeons' memory performance, nor did it affect response latency. These findings add to the growing evidence that, while effective at improving memory function in models of impaired memory, aniracetam has no effect in improving memory in healthy organisms.

Searching for Face-Category Representation in the Avian Visual Forebrain.

Visual information is processed hierarchically along a ventral ('what') pathway that terminates with categorical representation of biologically relevant visual percepts (such as faces) in the mammalian extrastriate visual cortex. How birds solve face and object representation without a neocortex is a long-standing problem in evolutionary neuroscience, though multiple lines of evidence suggest that these abilities arise from circuitry fundamentally similar to the extrastriate visual cortex. The aim of the present experiment was to determine whether birds also exhibit a categorical representation of the avian face-region in four visual forebrain structures of the tectofugal visual pathway: entopallium (ENTO), mesopallium ventrolaterale (MVL), nidopallium frontolaterale (NFL), and area temporo-parieto-occipitalis (TPO). We performed electrophysiological recordings from the right and left hemispheres of 13 pigeons while they performed a Go/No-Go task that required them to discriminate between two sets of stimuli that included images of pigeon faces. No neurons fired selectively to only faces in either ENTO, NFL, MVL, or TPO. Birds' predisposition to attend to the local-features of stimuli may influence the perception of faces as a global combination of features, and explain our observed absence of face-selective neurons. The implementation of naturalistic viewing paradigms in conjunction with electrophysiological and fMRI techniques has the potential to promote and uncover the global processing of visual objects to determine whether birds exhibit category-selective patches in the tectofugal visual forebrain.

Columban Simulation Project 2.0: Numerical Competence and Orthographic Processing in Pigeons and Primates.

Thirty years ago Burrhus Frederic Skinner and Robert Epstein began what is known as the Columban Simulation Project. With pigeons as their subjects, they simulated a series of studies that purportedly demonstrated insight, self-recognition, and symbolic communication in chimpanzees. In each case, with the appropriate training, they demonstrated that pigeons performed in a comparable manner to chimpanzees. When discussing these studies in the context of his Null Hypothesis, Macphail paid little attention to how the pigeons and chimpanzees solved the tasks and simply assumed that successful performance on the tasks reflected a similar underlying mechanism. Here, following a similar process to the original Columban Simulation Project, we go beyond this success testing and employ the signature testing approach to assess whether pigeons and primates employ a similar mechanism on tasks that tap numerical competence and orthographic processing. Consistent with the Null Hypothesis, pigeons and primates successfully passed novel transfer tests and, critically, displayed comparable cognitive signatures. While these findings demonstrate the absence of a qualitative difference, the time taken to train pigeons on these tasks revealed a clear quantitative difference.

Pigeons (Columba livia) learn a four-item list by trial and error.

The aim of the current study was to assess whether pigeons could acquire a four-item list by trial and error. Pigeons received either extensive list training prior to being tested on a novel four-item list (i.e., the full-training group) or very limited training (i.e., the limited-training group). Specifically, subjects in the full-training group were trained to acquire a large set of two-item lists by trial and error, then a large set of three-item lists, and finally a large set of four-item lists. In addition, within each set, the number of training phases was gradually reduced. In contrast, the limited-training group were trained on a single four-item list prior to testing. Only one of the eight subjects (12.5%) in the limited-training group learned the novel four-item list. In contrast, all five subjects (100%) in the full-training group learned the novel four-item list. We suggest that the difference between groups reflects the fact that subjects in the full-training group acquired a learning set over the course of their extensive training. The current study is the first to demonstrate pigeons can learn a four-item list without phased training. (PsycINFO Database Record

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.

Neurons in the Pigeon Nidopallium Caudolaterale Display Value-Related Activity.

We recorded from neurons in the nidopallium caudolaterale, the avian equivalent of the mammalian prefrontal cortex, in four birds. The birds were required to peck a stimulus that indicated the amount of reward they would receive (small or large) after a certain delay (short or long). We found that the activity of neurons in the nidopallium caudolaterale was modulated by the value of the reward that would be received based on the reward amount and the delay to reward. We found that value coding was most prominent during the presentation of the sample period, and less so during the delay period and during the presentation of the reward itself. Our findings support the view that activity in nidopallium caudolaterale reflects the encoding of the value of reward based on a combination of reward amount and delay to a reward.