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Birds exhibit two types of sleep that are in many respects similar to mammalian rapid eye movement (REM) and non-REM (NREM) sleep. As in mammals, several aspects of avian sleep can occur in a local manner within the brain. Electrophysiological evidence of NREM sleep occurring more deeply in one hemisphere, or only in one hemisphere – the latter being a phenomenon most pronounced in dolphins – was actually first described in birds. Such asymmetric or unihemispheric NREM sleep occurs with one eye open, enabling birds to visually monitor their environment for predators. Frigatebirds primarily engage in this form of sleep in flight, perhaps to avoid collisions with other birds. In addition to interhemispheric differences in NREM sleep intensity, the intensity of NREM sleep is homeostatically regulated in a local, use-depended manner within each hemisphere. Furthermore, the intensity and temporo-spatial distribution of NREM sleep-related slow waves varies across layers of the avian hyperpallium – a primary visual area – with the slow waves occurring first in, and propagating through and outward from, thalamic input layers. Slow waves also have the greatest amplitude in these layers. Although most research has focused on NREM sleep, there are also local aspects to avian REM sleep. REM sleep-related reductions in skeletal muscle tone appear largely restricted to muscles involved in maintaining head posture. Other local aspects of sleep manifest as a mixture of features of NREM and REM sleep occurring simultaneously in different parts of the neuroaxis. Like monotreme mammals, ostriches often exhibit brainstem-mediated features of REM sleep (muscle atonia and rapid eye movements) while the hyperpallium shows EEG slow waves typical of NREM sleep. Finally, although mice show slow waves in thalamic input layers of primary sensory cortices during REM sleep, this is not the case in the hyperpallium of pigeons, suggesting that this phenomenon is not a universal feature of REM sleep. Collectively, the local aspects of sleep described in birds and mammals reveal that wakefulness, NREM sleep, and REM sleep are not always discrete states.

Propagating slow-waves in electroencephalogram (EEG) or local field potential (LFP) recordings occur during non-rapid eye-movement (NREM) sleep in both mammals and birds. Moreover, in both, input from the thalamus is thought to contribute to the genesis of NREM sleep slow-waves. Interestingly, the general features of slow-waves are also found under isoflurane anesthesia. However, it is unclear to what extent these slow-waves reflect the same processes as those giving rise to NREM sleep slow-waves. Similar slow-wave spatio-temporal properties during NREM sleep and isoflurane anesthesia would suggest that both types of slow-waves are based on related processes. We used a 32-channel silicon probe connected to a transmitter to make intra-cortical recordings of the visual hyperpallium in naturally sleeping and isoflurane anesthetized pigeons (Columba livia) using a within-bird design. Under anesthesia, the amplitude of LFP slow-waves was higher when compared to NREM sleep. Spectral power density across all frequencies (1.5-100 Hz) was also elevated. In addition, slow-wave coherence between electrode sites was higher under anesthesia, indicating higher synchrony when compared to NREM sleep. Nonetheless, the spatial distribution of slow-waves under anesthesia was more comparable to NREM sleep than to wake or REM sleep. Similar to NREM sleep, slow-wave propagation under anesthesia mainly occurred in the thalamic input layers of the hyperpallium, regions which also showed the greatest slow-wave power during both recording conditions. This suggests that the thalamus could be involved in the genesis of slow-waves under both conditions. Taken together, although slow-waves under isoflurane anesthesia are stronger, they share spatio-temporal activity characteristics with slow-waves during NREM sleep.

Sleep’s role in memory consolidation is widely accepted. However, the role of the different sleep states and accompanying neurophysiological activity is still actively debated. Most theories of sleep-related memory consolidation are based on studies in a few mammalian species. Recent evidence from research in birds, which exhibit sleep states that are in most respects similar to those found in mammals (despite being distantly related) suggests that the way some types of memories are consolidated during sleep might be different in taxa other than mammals. This review will discuss how the recent sleep-related neurophysiological findings in birds inform our understanding of memory consolidation during sleep.

The current memory consolidation models suggest that the various brain rhythms (i.e. neocortical slow-waves, hippocampal sharp-wave ripples (SWRs) and thalamocortical spindles) occurring throughout the mammalian brain during sleep form an oscillatory network thought to be involved in the processing of information acquired during wakefulness. While sleep’s role in memory consolidation is widely accepted, the exact role of the different sleep states and accompanying neurophysiological activity is still actively debated. Most theories of sleep-related memory consolidation are solely based on studies in a few mammalian species. In contrast, virtually nothing is known about how the avian brain operates as a system during sleep and how this compares to what is known in mammals. In addition, though avian sleep has been implicated in various forms of memory consolidation, e.g. imprinting, song learning and in auditory memories, the existence and role of rhythms like thalamocortical spindles and hippocampal SWRs has not been studied in depth so far. In this thesis I investigated the neurophysiology of avian rapid eye-movement (REM) and non-REM (NREM) sleep, using intra-cortical recordings made with high-density electrode probes in anesthetized and naturally sleeping birds. I aimed to characterize the thalamocortical and hippocampal network activity underlying NREM and REM sleep in birds in order to deepen our understanding of the mechanisms and functions of avian sleep-related brain activity. I show that, as in mammals, traveling slow-waves are found in most of the avian pallium, both under isoflurane anesthesia and natural NREM sleep. Though, unlike mammals, slow-waves appear not to be present in the avian hippocampus. Moreover, the apparent absence of two of the rhythms (i.e. thalamocortical spindles and hippocampal SWRs), implicated in hippocampal memory transfer in mammals, questions whether hippocampal memory consolidation takes place during avian sleep. This result would fit with the fact that, even though the avian hippocampus is involved in storing certain types of information (e.g. spatial memories), there is so far no evidence for hippocampal memories being transferred to other brain regions in birds. I furthermore compared the neurophysiology of NREM sleep and isoflurane induced anesthesia using a within-bird design, in order to compare the underlying intra-cortical dynamics during these to recording conditions. I found that, though there are some spectral differences between these states, the similarities predominated, namely that travelling slow-waves are present in both NREM sleep and in the anesthetized brain regions examined. Taken together, the results from research in birds, which exhibit sleep states that are in most respects similar to those found in mammals (despite being distantly related), suggest that the way some types of memories are consolidated during sleep might be fundamentally different in taxa other than mammals.

Infants are thought to be sensitive to frequency in the input as a cue for phonological development. However, linguistic biases such as phonological markedness have been argued to play a role too. Since frequency and markedness are correlated, the two assertions could be different interpretations of data that confound frequency and markedness. In this study we disentangle the two, by testing infants’ preferences for syllables contrasting in frequency, balanced for markedness, and for syllables contrasting in markedness, balanced for frequency. We expected a developmental change from frequency-independent to frequency-dependent sensitivity. In addition, we expected an early preference for unmarked structure and a later preference for marked structures, as previously found in child language productions. We find that 9-month-olds prefer phonologically unmarked homorganic patterns, independent of frequency, whereas 12-month-olds prefer marked heterorganic patterns. In contrast to what we expected, only a weak effect for frequency is found and no developmental change.

Songbird vocal learning has interesting behavioural and neural parallels with speech acquisition in human infants. Zebra finch males sing one unique song that they imitate from conspecific males, and both sexes learn to recognize their father's song. Although males copy the stereotyped syllable sequence of their father's song, the role of sequential information in recognition remains unclear. Here, we investigated father's song recognition after changing the serial order of syllables (switching the middle syllables, first and last syllables, or playing all syllables in inverse order). Behavioural approach and call responses of adult male and female zebra finches to their father's versus unfamiliar songs in playback tests demonstrated significant recognition of father's song with all syllable-order manipulations. We then measured behavioural responses to normal versus inversed-order father's song. In line with our first results, the subjects did not differentiate between the two. Interestingly, when males' strength of song learning was taken into account, we found a significant correlation between song imitation scores and the approach responses to the father's song. These findings suggest that syllable sequence is not essential for recognition of father's song in zebra finches, but that it does affect responsiveness of males in proportion to the strength of vocal learning. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Both mammals and birds exhibit two sleep states, slow wave sleep (SWS) and rapid eye movement (REM) sleep. Studying certain aspects of sleep-related electrophysiology in freely behaving animals can present numerous methodological constraints, particularly when even fine body movements interfere with electrophysiological signals. Interestingly, under light general anesthesia, mammals and birds also exhibit slow waves similar to those observed during natural SWS. For these reasons, slow waves occurring under general anesthesia are commonly used in the investigation of sleep-related neurophysiology. However, how spectral properties of slow waves induced by anesthesia correspond to those occurring during natural SWS in birds has yet to be investigated systematically. In this study, we systematically analyzed spectral properties of electroencephalographic (EEG) patterns of pigeons (Columba livia) occurring under two commonly used anesthetics, isoflurane and urethane. These data were compared with EEG patterns during natural sleep. Slow waves occurring during spontaneous SWS, and those induced with isoflurane and urethane all showed greatest absolute power in the slowest frequencies (

Artificial grammar learning (AGL) has become an important tool used to understand aspects of human language learning and whether the abilities underlying learning may be unique to humans or found in other species. Successful learning is typically assumed when human or animal participants are able to distinguish stimuli generated by the grammar from those that are not at a level better than chance. However, the question remains as to what subjects actually learn in these experiments. Previous studies of AGL have frequently introduced multiple potential contributors to performance in the training and testing stimuli, but meta‐analysis techniques now enable us to consider these multiple information sources for their contribution to learning—enabling intended and unintended structures to be assessed simultaneously. We present a blueprint for meta‐analysis approaches to appraise the effect of learning in human and other animal studies for a series of artificial grammar learning experiments, focusing on studies that examine auditory and visual modalities. We identify a series of variables that differ across these studies, focusing on both structural and surface properties of the grammar, and characteristics of training and test regimes, and provide a first step in assessing the relative contribution of these design features of artificial grammars as well as species‐specific effects for learning., Studies of AGL have frequently used training and test stimuli that might provide multiple cues for learning, raising the question what subjects have actually learned. Using a selected subset of studies on humans and non‐human animals, Trotter et al. demonstrate how a meta‐analysis can be used to identify relevant experimental variables, providing a first step in asssessing the relative contribution of design features of grammars as well as of species‐specific effects on AGL.

Study Objectives: The changes in electroencephalogram (EEG) activity that characterize sleep and its sub-states-slow-wave sleep (SWS) and rapid eye movement (REM) sleep-are similar in mammals and birds. SWS is characterized by EEG slow waves resulting from the synchronous alternation of neuronal membrane potentials between hyperpolarized down-states with neuronal quiescence and depolarized up-states associated with action potentials. By contrast, studies of non-avian reptiles report the presence of high-voltage sharp waves (HShW) during sleep. How HShW relate to EEG phenomena occurring during mammalian and avian sleep is unclear. We investigated the spatiotemporal patterns of electrophysiological phenomena in Nile crocodiles (Crocodylus niloticus) anesthetized with isoflurane to determine whether they share similar spatiotemporal patterns to mammalian and avian slow waves. Methods: Recordings of anesthetized crocodiles were made using 64-channel penetrating arrays with electrodes arranged in an 8 × 8 equally spaced grid. The arrays were placed in the dorsal ventricular ridge (DVR), a region implicated in the genesis of HShW. Various aspects of the spatiotemporal distribution of recorded signals were investigated. Results: Recorded signals revealed the presence of HShW resembling those reported in earlier studies of naturally sleeping reptiles. HShW propagated in complex and variable patterns across the DVR. Conclusions: We demonstrate that HShW within the DVR propagate in complex patterns similar to those observed for avian slow waves recorded from homologous brain regions. Consequently, sleep with HShW may represent an ancestral form of SWS, characterized by up-states occurring less often and for a shorter duration than in mammals and birds.

The appearance of perineuronal nets (PNNs) represents one of the mechanisms that contribute to the closing of sensitive periods for neural plasticity. This relationship has mostly been studied in the ocular dominance model in rodents. Previous studies also indicated that PNN might control neural plasticity in the song control system of songbirds. To further elucidate this relationship, we quantified PNN expression and their localization around parvalbumin interneurons at key time-points during ontogeny in both male and female zebra finches, and correlated these data with the well-described development of song in this species. We also extended these analyses to the auditory system. The development of PNN during ontogeny correlated with song crystallization although the timing of PNN appearance in the four main telencephalic song control nuclei slightly varied between nuclei in agreement with the established role these nuclei play during song learning. Our data also indicate that very few PNN develop in the secondary auditory forebrain areas even in adult birds, which may allow constant adaptation to a changing acoustic environment by allowing synaptic reorganization during adulthood.

Sleep in birds is composed of two distinct sub-states, remarkably similar to mammalian slow-wave sleep (SWS) and rapid eye movement (REM) sleep. However, it is unclear whether all aspects of mammalian sleep are present in birds. We examined whether birds suppress REM sleep in response to changes in sleeping conditions that presumably evoke an increase in perceived predation risk, as observed previously in rodents. Although pigeons sometimes sleep on the ground, they prefer to sleep on elevated perches at night, probably to avoid nocturnal mammalian ground predators. Few studies to date have investigated how roosting sites affect sleep architecture. We compared sleep in captive pigeons on days with and without access to high perches. On the first (baseline) day, low and high perches were available; on the second day, the high perches were removed; and on the third (recovery) day, the high perches were returned. The total time spent sleeping did not vary significantly between conditions; however, the time spent in REM sleep declined on the low-perch night and increased above baseline when the pigeons slept on the high perch during the recovery night. Although the amount of SWS did not vary significantly between conditions, SWS intensity was lower on the low-perch night, particularly early in the night. The similarity of these responses between birds and mammals suggests that REM sleep is influenced by at least some ecological factors in a similar manner in both groups of animals.

Following Jerry Hogan, I argue that questions of function and evolution, and questions of mechanism should be seen as logically distinct. Evolution is concerned with a historical reconstruction of traits, while the actual underlying mechanisms are the domain of cognitive neuroscience and psychology. Functional and evolutionary considerations may be used to generate hypotheses regarding the underlying mechanisms. But these hypotheses may be false and should always be tested empirically. Many researchers still hold that common descent implies cognitive closeness. Studies on birds suggest that evolutionary convergence may be the rule rather than the exception in animal cognition. Neurocognitive differences between classes of individuals are often thought to be the result of adaptive specialisation. In the case of learning and memory, however, empirical results are more consistent with a 'general process' interpretation, without qualitative differences between different taxa. Evolutionary psychology (EP) argues that the mind of modern humans was formed as a result of selection pressures in the Stone Age. The empirical data are often overinterpreted, and EP is mostly based upon an outdated view of evolutionary biology. In human speech and language, both neurogenetic homology and evolutionary convergence are involved regarding speech, but human language has a unique combinatorial complexity. This article is part of a Special Issue entitled: In Honor of Jerry Hogan.

Several mammalian-based theories propose that the varying patterns of neuronal activity occurring in wakefulness and sleep reflect different modes of information processing. Neocortical slow-waves, hippocampal sharp-wave ripples, and thalamocortical spindles occurring during mammalian non-rapid eye-movement (NREM) sleep are proposed to play a role in systems-level memory consolidation. Birds show similar NREM and REM (rapid eye-movement) sleep stages to mammals; however, it is unclear whether all neurophysiological rhythms implicated in mammalian memory consolidation are also present. Moreover, it is unknown whether the propagation of slow-waves described in the mammalian neocortex occurs in the avian "cortex" during natural NREM sleep. We used a 32-channel silicon probe connected to a transmitter to make intracerebral recordings of the visual hyperpallium and thalamus in naturally sleeping pigeons (Columba livia). As in the mammalian neocortex, slow-waves during NREM sleep propagated through the hyperpallium. Propagation primarily occurred in the thalamic input layers of the hyperpallium, regions that also showed the greatest slow-wave activity (SWA). Spindles were not detected in both the visual hyperpallium, including regions receiving thalamic input, and thalamus, using a recording method that readily detects spindles in mammals. Interestingly, during REM sleep fast gamma bursts in the hyperpallium (when present) were restricted to the thalamic input layers. In addition, unlike mice, the decrease in SWA from NREM to REM sleep was the greatest in these layers. Taken together, these variant and invariant neurophysiological aspects of avian and mammalian sleep suggest that there may be associated mechanistic and functional similarities and differences between avian and mammalian sleep.

The faculty of language is thought to be uniquely human. Recently, it has been claimed that songbirds are able to associate meaning with sound, comparable to the way that humans do. In human language, the meaning of expressions (semantics) is dependent on a mind-internal hierarchical structure (syntax). Meaning is associated with structure through the principle of compositionality, whereby the meaning of a complex expression is a function of the meaning of its constituent parts and the mode of composition. We argue that while recent experimental findings on songbird call sequences offer exciting novel insights into animal communication, despite claims to the contrary, they are quite unlike what we find in human language. There are indeed remarkable behavioral and neural parallels in auditory-vocal imitation learning between songbirds and human infants that are absent in our closest evolutionary relatives, the great apes. But so far, there is no convincing evidence of syntax-determined meaning in nonhuman animals.

This special issue of Behavioural Processes is dedicated to the contributions of Jerry A. Hogan to behavioural biology—or ‘ethology’ as this field used to be known. These contributions are manifold, and have inspired many researchers, not only in ethology, but also in experimental psychology and behavioural neuroscience, as can be seen from the different contributions to this issue. Hogan has conducted pioneering research into the causation and development of animal behaviour. In addition, he has written extensively on the theoretical foundations of the field. In particular, he has emphasised the logical distinction between cause and function in behavioural biology. This is a fundamental distinction, and its misinterpretations have often led the field astray. That this discussion is still ongoing is exemplified in several papers in the present issue (Lefebvre, 2015, Bolhuis, 2015 and Laland, 2015).

The zebra finch (Taeniopygia guttata) song control system consists of several series of interconnected brain nuclei that undergo marked changes during ontogeny and sexual development, making it an excellent model to study developmental neuroplasticity. Despite the demonstrated influence of hormones such as sex steroids on this phenomenon, thyroid hormones (THs) - an important factor in neural development and maturation - have not been studied in this regard. We used in situ hybridization to compare the expression of TH transporters, deiodinases and receptors between both sexes during all phases of song development in male zebra finch. Comparisons were made in four song control nuclei: Area X, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), HVC (used as proper name) and the robust nucleus of the arcopallium (RA). Most genes regulating TH action are expressed in these four nuclei at early stages of development. However, while general expression levels decrease with age, the activating enzyme deiodinase type 2 remains highly expressed in Area X, HVC and RA in males, but not in females, until 90days post-hatch (dph), which marks the end of sensorimotor learning. Furthermore, the L-type amino acid transporter 1 and TH receptor beta show elevated expression in male HVC and RA respectively compared to surrounding tissue until adulthood. Differences compared to surrounding tissue and between sexes for the other TH regulators were minor. These developmental changes are accompanied by a strong local increase in vascularization in the male RA between 20 and 30dph but not in Area X or HVC. Our results suggest that local regulation of TH signaling is an important factor in the development of the song control nuclei during the song learning phase and that TH activation by DIO2 is a key player in this process.

Vocalisation in songbirds and parrots has become a prominent model system for speech and language in humans. We investigated possible sex differences in behavioural and neural responsiveness to mate calls in the budgerigar, a vocally-learning parrot. Males and females were paired for 5 weeks and then separated, after which we measured vocal responsiveness to playback calls (a call of their mate versus a call of an unfamiliar conspecific). Both sexes learned to recognise mate calls during the pairing period. In males, but not females, mate calls evoked significantly fewer vocal responses than unfamiliar calls at one month after separation. Furthermore, in females, there was significantly greater molecular neuronal activation in response to mate calls compared to silence in the caudomedial mesopallium (CMM), a higher-order auditory region, in both brain hemispheres. In males, we found right-sided dominance of molecular neuronal activation in response to mate calls in the CMM. This is the first evidence suggesting sex differences in functional asymmetry of brain regions related to recognition of learned vocalisation in birds. Thus, sex differences related to recognition of learned vocalisations may be found at the behavioural and neural levels in avian vocal learners as it is in humans.

Learned bird songs are often characterized by a high degree of variation between individuals and sometimes between populations, while at the same time maintaining species specificity. The evolution of such songs depends on the balance between plasticity and constraints. Captive populations provide an opportunity to examine signal variation and differentiation in detail, so we analyzed adult male zebra finch (Taeniopygia guttata) songs recorded from 13 populations across the world, including one sample of songs from wild-caught males in their native Australia. Cluster analysis suggested some, albeit limited, evidence that zebra finch song units belonged to universal, species-wide categories, linked to restrictions in vocal production and non-song parts of the vocal repertoire. Across populations, songs also showed some syntactical structure, although any song unit could be placed anywhere within the song. On the other hand, there was a statistically significant differentiation between populations, but the effect size was very small, and its communicative significance dubious. Our results suggest that variation in zebra finch songs within a population is largely determined by species-wide constraints rather than population-specific features. Although captive zebra finch populations have been sufficiently isolated to allow them to genetically diverge, there does not appear to have been any divergence in the genetically determined constraints that underlie song learning. Perhaps more surprising is the lack of locally diverged cultural traditions. Zebra finches serve as an example of a system where frequent learning errors may rapidly create within-population diversity, within broad phonological and syntactical constraints, and prevent the formation of long-term cultural traditions that allow populations to diverge.

The dichotomy between 'typological thinking' and 'population thinking' features in a range of debates in contemporary and historical biology. The origins of this dichotomy are often traced to Ernst Mayr, who is said to have coined it in the 1950s as a rhetorical device that could be used to shield the Modern Synthesis from attacks by the opponents of population biology. In this two-part essay I argue that the origins of the typology/population dichotomy are considerably more complicated and more interesting than is commonly thought. In this first part, I will argue that Mayr's dichotomy was based on two distinct type/population contrasts that had been articulated much earlier by George Gaylord Simpson and Theodosius Dobzhansky. Their distinctions made eminent sense in their own, isolated contexts. In the second part, I will show how Mayr conflated these type/population distinctions and blended in some of his own, unrelated concerns with 'types' of a rather different sort. Although Mayr told his early critics that he was merely making "a temporary oversimplification," he ended up burdening the history and philosophy of biology with a troubled dichotomy.

Brain rhythms occurring during sleep are implicated in processing information acquired during wakefulness, but this phenomenon has almost exclusively been studied in mammals. In this review we discuss the potential value of utilizing birds to elucidate the functions and underlying mechanisms of such brain rhythms. Birds are of particular interest from a comparative perspective because even though neurons in the avian brain homologous to mammalian neocortical neurons are arranged in a nuclear, rather than a laminar manner, the avian brain generates mammalian-like sleep-states and associated brain rhythms. Nonetheless, until recently, this nuclear organization also posed technical challenges, as the standard surface EEG recording methods used to study the neocortex provide only a superficial view of the sleeping avian brain. The recent development of high-density multielectrode recording methods now provides access to sleep-related brain activity occurring deep in the avian brain. Finally, we discuss how intracerebral electrical imaging based on this technique can be used to elucidate the systems-level processing of hippocampal-dependent and imprinting memories in birds.

Large morphological sex differences in the vertebrate brain were initially identified in song control nuclei of oscines. Besides gross differences between volumes of nuclei in males and females, sex differences also concern the size and dendritic arborization of neurons and various neurochemical markers, such as the calcium-binding protein parvalbumin (PV). Perineuronal nets (PNN) of the extracellular matrix are aggregates of different compounds, mainly chondroitin sulfate proteoglycans, that surround subsets of neurons, often expressing PV. PNN develop in zebra finches song control nuclei around the end of the sensitive period for song learning and tutor deprivation, known to delay the end of the song learning sensitive period, decreases the numbers of PNN in HVC. We demonstrate here the existence in zebra finches of a major sex difference (males > females) affecting the number of PNN (especially those surrounding PV-positive cells) in HVC and to a smaller extent the robust nucleus of the arcopallium, RA, the two main nuclei controlling song production. These differences were not present in Area X and LMAN, the lateral magnocellular nucleus of the anterior nidopallium. A dense expression of material immunoreactive for chondroitin sulfate was also detected in several nuclei of the auditory and visual pathways. This material was often organized in perineuronal rings but quantification of these PNN did not reveal any sex difference with the exception that the percentage of PNN surrounding PV-ir cells in the dorsal lateral mesencephalic nucleus, MLd, was larger in females than in males, a sex difference in the opposite direction compared to what is seen in HVC and RA. These data confirm and extend previous studies demonstrating the sex difference affecting PNN in HVC-RA by showing that this sex difference is anatomically specific and does not concern visual or auditory pathways.