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Relative size of the medial and lateral pontine nuclei (PM, PL). (A,B) The log-transformed volume of the PM and PL is plotted as a function of the brain volume minus the volume of each structure (PM = A; PL = B) for all species examined (see methods and supplementary materials, Table S1). Parrots (Psittaciformes) are shown in red. (C,D) Box plots show the relative size of PM (C) and PL (D) for each avian orders represented in this study. Parrots (Psittaciformes), are shown in red. Values shown in the box plots are derived from the residuals from PGLS of the log of the volume of each nucleus against the brain volume (see methods, panel A,B). The solid horizontal line represents the median, the two boxes represent the limits of the second and third quartiles and the whiskers (dashed vertical lines) represent the limits of the first and fourth quartiles. The open circles represent outliers, which are defined as those outside the first or fourth quartile by a magnitude of 1.5X the inter-quartile range. An = Anseriformes, Ch = Charadriiformes, Co = Columbiformes, F = Falconiformes, G = Galliformes, Gr = Gruiformes, Pa = Passeriformes, Pal = Paleognaths, Pe = Pelecaniformes, Pi = Piciformes, Pr = Procellariiformes, Ps = Psittaciformes, St = Strigiformes, Tr = Trochiliformes.
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It is widely accepted that parrots show remarkable cognitive abilities. In mammals, the evolution of complex cognitive abilities is associated with increases in the size of the telencephalon and cerebellum as well as the pontine nuclei, which connect these two regions. Parrots have relatively large telencephalons that rival those of primates, but w...
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... A similar situation can be observed in parrots. These birds probably display the highest avian telencephalic neuron counts (Kverkov a et al., 2022;Olkowicz et al., 2016;Ströckens et al., 2022), and a greatly enlarged medial spiriform nucleus, which acts as an interface between the pallium and the cerebellum, enabling enhanced motor cognition (Gutiérrez-Ib añez et al., 2018). However, the Tanimbar corella (Cacatua goffiniana) is the only parrot known to be a sophisticated tool user in the wild (O'Hara et al., 2021); tellingly, the Tanimbar corella also inhabits an isolated Indonesian archipelago. ...
Recent years have seen increasing scientific interest in whether neuron counts can act as correlates of diverse biological phenomena. Lately, Herculano-Houzel (2023) argued that fossil endocasts and comparative neurological data from extant sauropsids allow to reconstruct telencephalic neuron counts in Mesozoic dinosaurs and pterosaurs, which might act as proxies for behaviors and life history traits in these animals. According to this analysis, large theropods such as Tyrannosaurus rex were long-lived, exceptionally intelligent animals equipped with “macaque- or baboon-like cognition”, whereas sauropods and most ornithischian dinosaurs would have displayed significantly smaller brains and an ectothermic physiology. Besides challenging established views on Mesozoic dinosaur biology, these claims raise questions on whether neuron count estimates could benefit research on fossil animals in general. Here, we address these findings by revisiting Herculano-Houzel's (2023) work, identifying several crucial shortcomings regarding analysis and interpretation. We present revised estimates of encephalization and telencephalic neuron counts in dinosaurs, which we derive from phylogenetically informed modeling and an amended dataset of endocranial measurements. For large-bodied theropods in particular, we recover significantly lower neuron counts than previously proposed. Furthermore, we review the suitability of neurological variables such as neuron numbers and relative brain size to predict cognitive complexity, metabolic rate and life history traits in dinosaurs, coming to the conclusion that they are flawed proxies for these biological phenomena. Instead of relying on such neurological estimates when reconstructing Mesozoic dinosaur biology, we argue that integrative studies are needed to approach this complex subject.
... 5 In species where both sexes sing, while less studied, 6 the HPG axis appears to play a similar role in shaping brain and singing behavior in both sexes. [7][8][9][10] Parrots are closely related to songbirds 11 yet independently evolved different vocal tract structures; 12 different steroid receptor distributions in the brain; 13 different, more elaborate vocal control circuits in the telencephalon [14][15][16][17] and both sexes use vocal plasticity in a broader suite of non-reproductive functions. [18][19][20] However, the neuroendocrinology of parrots has been less studied, 5,21 and we lack an understanding of how the endocrine system coordinates the development of vocal learning in non-songbirds in ways that are adaptive, 22,23 which may bias our understanding of how neuroendocrine networks foster complex vocal communication in parrots other groups. ...
... 1,5 These and other studies have led some to suggest the oscine song system is a highly specialized brain module that might help explain its success across oscines, 1,13,24 whereas parrots have a more distributed, primate-like telencephalic-midbrain-cerebellar loop and reduplicated vocal control circuits in the telencephalon, both of which are implicated in complex social communication and cognition. 15,16 Importantly, exogenous T activated male phenotypes in female budgerigars after sexual maturation and led the authors to suggest that the development of vocal learning circuitry in parrots does not depend on early organizational effects of androgens or estrogens, though this needs testing. Because the HPG axis becomes functional around sexual maturation, endogenous production of gonadal steroids is likely limited (e.g., mini-puberty) 28 during the nestling phase and thus major period of growth and maturation in altricial songbirds and parrots. ...
... Nest ID was included as a random effect in the model, to control for repeated measures of nestlings in the same nest. Vocal output, CORT treatment, CORT treatment phase (13)(14)(15)(16)(17)(18)(19) vs. 20-26 dph), vocal phase of babbling (20-27 vs. 28-36 dph), sex, age, hatch sequence, and brood size were included as fixed effects. ...
The neuroendocrinology of vocal learning is exceptionally well known in passerine songbirds. Despite huge life history, genetic and ecological variation across passerines, song learning tends to occur as a result of rises in gonadal and non‐gonadal sex steroids that shape telencephalic vocal control circuits and song. Parrots are closely related but independently evolved different cerebral circuits for vocal repertoire acquisition in both sexes that serve a broader suite of social functions and do not appear to be shaped by early androgens or estrogens; instead, parrots begin a plastic phase in vocal development at an earlier life history stage that favors the growth, maturation, and survival functions of corticosteroids. As evidence, corticosterone (CORT) supplements given to wild green‐rumped parrotlets ( Forpus passerinus ) during the first week of vocal babbling resulted in larger vocal repertoires in both sexes in the remaining days before fledging. Here, we replicate this experiment but began treatment 1 week before in development, analyzing both experiments in one model and a stronger test of the organizational effects of CORT on repertoire acquisition. Early CORT treatment resulted in significantly larger repertoires compared to late treatment. Both treatment groups showed weak negative effects on the early, reduplicated stage of babbling and strong, positive effects of CORT on the later, variegated stage. Results are consistent with more formative effects of corticosteroids at earlier developmental stages and a role of the hypothalamic–pituitary–adrenal axis (HPA) in vocal repertoire acquisition. Given the early emergence of speech in human ontogeny, parrots are a promising model for understanding the putative role of the HPA axis in the construction of neural circuits that support language acquisition.
... Box 3. Putative further candidates for complex cognition A potential future candidate for complex cognition is the cerebellum, which is tightly connected to cognitive processes in humans [118]. Parrots not only have excellent cognition but also a drastically enlarged avian-specific midbrain structure that serves as a link between the arcopallium, a premotor structure, and the cerebellum [119]. This corresponds to the enlargement of the mammalian pontine nuclei, which are especially large in great apes. ...
Many cognitive neuroscientists believe that both a large brain and an isocortex are crucial for complex cognition. Yet corvids and parrots possess non-cortical brains of just 1–25 g, and these birds exhibit cognitive abilities comparable with those of great apes such as chimpanzees, which have brains of about 400 g. This opinion explores how this cognitive equivalence is possible. We propose four features that may be required for complex cognition: a large number of associative pallial neurons, a prefrontal cortex (PFC)-like area, a dense dopaminergic innervation of association areas, and dynamic neurophysiological fundaments for working memory. These four neural features have convergently evolved and may therefore represent ‘hard to replace’ mechanisms enabling complex cognition.
... » BM (λ = 0.0 (star-phylogeny); AIC = 6267. 87 Time to present (in million years) Fig. 1 Consensus phylogenetic tree for the 34 primate species in this study. We obtained the consensus tree for the 34 species in our dataset from 10kTrees Arnold et al. 142 . ...
... In the current work, we studied cerebellar volumes for 34 primate species (N = 63) and ansiform volumes for 13 species (N = 30). The cerebellum, and the ansiform specifically, are part of important cerebello-cerebral loops and networks contributing to transmodal, integrative functions [12][13][14]31,39,45,46,50,61,62,69,87,88 . ...
... Small timing differences in cell division cycles have been found to explain hyperscaling of (neo)cortical surface area in primates 106 . Common neurodevelopmental mechanisms may thus underlie both tight cerebello-cerebral scaling across vertebrates 31,32,34,71,87,88 and modular ansiform expansions 107 , suggesting two prominent evolutionary theories 49,104 are not mutually exclusive 50 . ...
The reciprocal connections between the cerebellum and the cerebrum have been suggested to simultaneously play a role in brain size increase and to support a broad array of brain functions in primates. The cerebello-cerebral system has undergone marked functionally relevant reorganization. In particular, the lateral cerebellar lobules crura I-II (the ansiform) have been suggested to be expanded in hominoids. Here, we manually segmented 63 cerebella (34 primate species; 9 infraorders) and 30 ansiforms (13 species; 8 infraorders) to understand how their volumes have evolved over the primate lineage. Together, our analyses support proportional cerebellar-cerebral scaling, whereas ansiforms have expanded faster than the cerebellum and cerebrum. We did not find different scaling between strepsirrhines and haplorhines, nor between apes and non-apes. In sum, our study shows primate-general structural reorganization of the ansiform, relative to the cerebello-cerebral system, which is relevant for specialized brain functions in an evolutionary context.
... Indeed, not only are parrots strong positive outliers among vertebrates in their relative brain sizes [83][84][85][86], but they possess a neuron density almost two-times that of mammals with similarly sized brains [87]. Thus, in many regards it has been suggested that the brains of parrots functionally resemble those of higher primates [55,77,[87][88][89]. ...
Parrots (Order: Psittaciformes) represent one of the most striking and ecomorphologically diverse avian clades, spanning more than two orders of magnitude in body size with populations occupying six continents. The worldwide diaspora of parrots is largely due to the pet trade, driven by human desire for bright, colorful, and intelligent animals as companions. Some introduced species have aptly inserted themselves into the local ecosystem and established successful breeding colonies all around the globe. Notably, the United States is home to several thriving populations of introduced species including red-masked parakeets (Psittacara erythrogenys), monk parakeets (Myiopsitta monachus), nanday conures (Aratinga nenday), and red-crowned amazons (Amazona viridigenalis). Their incredible success globally begs the question as to how these birds adapt so readily to novel environments. In this commentary, we trace parrots through evolutionary history, contextualize existent naturalized parrot populations within the contiguous United States, and provide a phylogenetic regression analysis of body mass and brain size based on success in establishing breeding populations. The propensity for a parrot species to become established appears to be phylogenetically driven. Notably, parrots in the family Cacatuidae and Neotropical Pyrrhua appear to be poor at establishing themselves in the United States once released. Although brain size among Psittaciformes did not show a significant impact on successful breeding in the continental United States, we propose that the success of parrots can be attributed to their charismatic nature, significant intelligence relative to other avian lineages, and behavioral flexibility.
... Therefore, high NWBM and NWBV in Aves as observed in this study points to the increased cognition compared to reptiles. The expansion of avian brain is directly linked with the highly coordinated activity of flight, manipulative motor activity involved in building nests [16], tool manufacture, vocal learning [23] and many other high cognitive performances. Moreover, studies in humans have shown that cerebellar volume accounts for variance in cognitive performance [24]. ...
Background: Motor coordination in vertebrates is primarily regulated by cerebellum. Divergence of Aves from reptilian ancestors results in noticeable improvement in the motor coordination. This study aims to explore anatomical innovations in the cerebellar cortex during the course of evolution of reptiles and Aves. Methods: Three representative species each from reptilian and avian lineages were selected to represent both vertebrate classes. Complete brain was dissected out from the cranial cavity of each specimen after radiological assessment of its extent. After gross examination, the brains were subjected to detailed histological investigation using conventional and special strains. Micrometry of layer and cellular architecture of cerebellar cortex were undertaken digitally using ImageJ and statistically compared using GraphPad Prism. Results: Grossly, significant increase (p<0.0001) in brain mass, brain volume and cerebellar volume was observed in Aves compared to reptiles. Histo-morphometric analyses of granular and molecular layers of cerebellum showed statistically significant decrease (p<0.0001) in the thickness of avian representatives compared to reptilian counterparts. Similarly significant decrease (p<0.0001) in the Inter-Purkinje neuronal distance was observed in Aves compared to reptiles. Conversely, increase cellular and neuronal count (p=0.0332 to <0.0001) count was observed in all three layers of avian cerebellum in comparison to reptiles. This suggests increased cellular packaging and/or density in the avian cerebellum compared to reptiles. Conclusion: In summary, significant increase in the cellular density and differentiation in the cerebellum of avian representatives may provide anatomical basis of increased motor coordination in Aves compared to reptiles. B Abstract www.als-journal.com/ RQ, Sharafat S (2023). Anatomical transition of trilaminar cerebellar cortex between reptiles and Aves. Adv. Life Sci. 10(2): 259-264.
... Psittaciformes are highly social with primate-like cognitive capacities (Olkowicz et al., 2016;Gutiérrez-Ibáñez et al., 2018;Emery, 2016). Despite being wild non-domesticated animals, they form strong affiliative bonds with people when captive (Baker, 2012;Anderson, 2014;Bond and Diamond, 2019). ...
In mammals, human-animal bonding is recognized as a source of positive affect for companion or farm animals. Because this remains unexplored in birds, we investigated captive parrots' perspective of the human-animal relationship. We used a classical separation-reunion paradigm and predicted that variations in parrots' facial displays and behaviours would indicate their appraisal of the relationship. The test was divided into three phases of two minutes each: the bird was placed in an unfamiliar environment with a familiar caregiver (union), then the bird was left alone (separation) and finally, the caregiver returned (reunion). The test was repeated 10 times for each bird and video recorded in order to analyze their behaviour. The data show significantly higher crown and nape feather heights, higher redness of the skin and higher frequency of contact-seeking behaviours during the union and reunion phases than during the separation phase during which they expressed long distance contact calls. We observed the expression of eye pinning during the union and reunion phases in one out of five macaws. We argue that variation in facial displays provides indicators of parrot's positive appraisal of the caretaker presence. Our results broaden the scope for further studies on parrots' expression of their subjective feelings.
... Multiple findings suggest neuronal specialization for vocal learning and motor control in parrots: the medial spiriform nucleus (SpM) of parrots is greatly enlarged compared to other avian species. It connects the telencephalon with the cerebellum and is believed to be integral for the deliberate control of fine motor skills and complex cognitive processes in a way that it is functionally analogous to the cortico-ponto-cerebellar pathways of mammals (Gutiérrez-Ibáñez et al. 2018). Additionally, the cerebellum (believed to play an essential role in complex motor behaviors) is more foliated in parrots, corvids, and seabirds than in other bird species (Iwaniuk et al. 2006). ...
Psittacines, along with corvids, are commonly referred to as ‘feathered apes’ due to their advanced cognitive abilities. Until rather recently, the research effort on parrot cognition was lagging behind that on corvids, however current developments show that the number of parrot studies is steadily increasing. In 2018, M. L. Lambert et al. provided a comprehensive review on the status of the most important work done so far in parrot and corvid cognition. Nevertheless, only a little more than 4 years after this publication, more than 50 new parrot studies have been published, some of them chartering completely new territory. On the 25th anniversary of Animal Cognition we think this warrants a detailed review of parrot cognition research over the last 4 years. We aim to capture recent developments and current trends in this rapidly expanding and diversifying field.
... This is an interesting finding considering the evolutionary distance between mammals and birds. Birds also have differently structured brains compared to mammals although their forebrain (nido-and mesopallium) represents a homologous structure to the mammalian neocortex 28,[46][47][48] . Like the neocortex, this telencephalic structure fulfills higher cognitive functions even if it lacks the cortex-typical lamination and is structured differently 49 . ...
The ability to recall one’s past actions is a crucial prerequisite for mental self-representation and episodic memory. We studied whether blue-throated macaws, a social macaw species, can remember their previous actions. The parrots were trained to repeat four previously learned actions upon command. Test sessions included repeat trials, double repeat trials and trials without repeat intermixed to test if the parrots repeated correctly, only when requested and not relying on a representation of the last behavioral command. Following their success, the parrots also received sessions with increasing time delays preceding the repeat command and successfully mastered 12–15 s delays. The parrots successfully transferred the repeat command spontaneously at first trial to three newly trained behaviors they had never repeated before, and also succeeded in a second trial intermixed with already trained actions (untrained repeat tests). This corroborates that successful repeating is not just an artifact of intense training but that blue-throated macaws can transfer the abstract “repeat rule” to untrained action. It also implies that an important aspect of self-representation has evolved in this avian group and might be adaptive, which is consistent with the complex socio-ecological environment of parrots and previous demonstrations of their complex cognition.
... in primates [61,73], as well as in cetaceans [83] and parrots [84]. Now, with elaborate phylogenetic techniques and additional neuroscientific tools, investigation of the non-motor CCS can be further substantiated. ...
... The CCS has been proposed to be among the evolutionary correlates of non-motor functions across a wide range of species [20,[83][84][85][86]. In primates, the system has undergone distinct adaptations. ...
... Differences in relative cerebellar volumes may stem from ecological factors [96,99] that may be related to cognitive ability [96,98]. Parrots have also developed a primate-like CCS [84]. This raises the question whether the CCS is also involved in supporting abstract cognitive abilities in parrots, such as logical reasoning [93], as the CCS is suited for supporting non-motor functions [13,20,21,100,101]. ...
The longstanding idea that the cerebral cortex is the main neural correlate of human cognition can be elaborated by comparative analyses along the vertebrate phylogenetic tree that support the view that the cerebello-cerebral system is suited to support non-motor functions more generally. In humans, diverse accounts have illustrated cerebellar involvement in cognitive functions. Although the neocortex, and its transmodal association cortices such as the prefrontal cortex, have become disproportionately large over primate evolution specifically, human neocortical volume does not appear to be exceptional relative to the variability within primates. Rather, several lines of evidence indicate that the exceptional volumetric increase of the lateral cerebellum in conjunction with its connectivity with the cerebral cortical system may be linked to non-motor functions and mental operation in primates. This idea is supported by diverging cerebello-cerebral adaptations that potentially coevolve with cognitive abilities across other vertebrates such as dolphins, parrots, and elephants. Modular adaptations upon the vertebrate cerebello-cerebral system may thus help better understand the neuroevolutionary trajectory of the primate brain and its relation to cognition in humans. Lateral cerebellar lobules crura I-II and their reciprocal connections to the cerebral cortical association areas appear to have substantially expanded in great apes, and humans. This, along with the notable increase in the ventral portions of the dentate nucleus and a shift to increased relative prefrontal-cerebellar connectivity, suggests that modular cerebellar adaptations support cognitive functions in humans. In sum, we show how comparative neuroscience provides new avenues to broaden our understanding of cerebellar and cerebello-cerebral functions in the context of cognition.
