Parrots and primates show impressive convergence of complex cognitive abilities1,2 and this is accompanied by convergent changes in the brain, such as: relatively large brains6,16,17, relatively large telencephalons26 and particularly large associative areas of the telencephalon31. Our results show an additional convergence between these two groups. We found that SpM, a nucleus that acts as a relay between the forebrain and the cerebellum, is particularly large in parrots compared to other birds (Table S3 and Fig. 2), and that the relative size of SpM is strongly correlated with the relative size of the telencephalon across all birds (Table 1). While this parallels the situation in primates, in so far that the size of the cortex is strongly correlated with that of the pons9,15, our results suggest, at most, a weak correlation between the relative size of SpM and the cerebellum. Nonetheless, this accounts for an impressive case of convergent evolution because SpM is not part of the pons, but rather located in the dorsal part of the border between the thalamus and pretectum20,25. Mammals do not have a comparable nucleus and among vertebrates, only teleosts have similar thalamic/pretectal nuclei that connect the forebrain with the cerebellum20,32. Our results also show that while the relative size of the pontine nuclei show some correlation with that of the cerebellum, these nuclei are not enlarged in parrots, (Tables S4 and S5). Thus, parrots and primates have convergently evolved increased connectivity between the telencephalon and the cerebellum, but have done so through different neural pathways.

The similarities in the evolution of cortico-cerebellar pathways between parrots and primates is not at all levels. While primates have a relative large cerebellum when compared to other mammals11, previous studies and our results show that parrots do not have a larger cerebellum than other birds (see results16). Despite the lack of an enlarged cerebellum in parrots, we did find a correlation between the relative size of the telencephalon and the cerebellum across all birds (see results), which seems to mimic the situation in primates and mammals9,11. However, this result should be interpreted with caution. In this study we compared the size of the whole telencephalon with that of the cerebellum while in mammals the comparison has been between the cortex and the cerebellum. It is possible that the inclusion of the pallium and sub-pallium in our data has affected our results, and that the relative size of the pallium is not correlated to that of the cerebellum in birds. Interestingly, parrots do show some differences in the cerebellum when compared to other birds. Previous research has shown that, relative to their brain size, parrots have more folded cerebella when compared to other birds33. It is therefore possible that the relative size of SpM is correlated to other aspect of cerebellar anatomy, such as the number or size of Purkinje cells.

The differences in the evolution of cortico-cerebellar pathways, particularly the cerebellum, between parrots and primates is not completely surprising given several major differences in the cerebellum of birds and mammals. The most prominent is the absence of a clear homologues of the cerebellar hemispheres in birds and their main output, the dentate nucleus34. This may be particularly relevant to the evolution of cortico-cerebellar pathways in birds, given that the main output of the dentate nucleus is regions of the thalamus that then projects to the cortex10, and these are precisely the components of the cerebellum that are enlarged in primates14,15. Also, while the cerebellum of primates contains up to 80% of the total number of cells in the brain35, in parrots the cerebellum only contains 40% or less of the total number of neurons in the brain, which results in a much lower ratio of cerebellar to pallial neurons in birds than mammals36. Further, the ratio between pallial and cerebellar cells is constant across all mammals, but varies among avian groups (see below, Fig. 4). This suggests that even though there are compelling convergences between birds and mammals in brain morphology and behavior, there are also some fundamental differences in how their brains are constructed. The implications of these differences for cognition are as yet unknown.

Figure 4 Scatterplot of the number of cells in the cerebellum of several species of birds versus the number of neurons in the pallium. Data from36. Full size image

While we did not find an expansion of the cerebellum or the pontine nuclei in parrots, our results suggest that across all birds exists a correlation between the size of these structures and the telencephalon. The correlation between the cerebellum and the telencephalon does not only mimics that found in primates (see above), but also in sharks37, which suggest that a correlated evolution of this two structures maybe wide spread among vertebrates. Additionally, the concerted evolution of the size of these two structures with that the pontine nuclei and SpM is similar to the correlated evolution of functional circuits in other systems of the avian brain, including the tectofugal pathway, other sensory pathways, and the song system38,39,40,41, as well to the correlated evolution of functional circuits in the brain of mammals9,11. This further supports the notion that interconnected structures evolve together and that neural circuits should be taken in consideration when studying the evolution of the brain.

Correlation between SpM and telencephalon

In primates, the expansion of the neocortex has been accompanied by the enlargement of existing areas and addition of new ones, in both primary sensory areas, mostly visual, and also sensorimotor, premotor and motor areas42,43. Sayol et al.31 has recently shown that the expansion of the telencephalon in parrots and corvids is mostly explained by an expansion of the associative pallium (AP), which they defined as the nidopallium and mesopallium plus its main output, the arcopallium. The AP contains both primary sensory circuits (visual, auditory, trigeminal-somatosensory), as well as premotor/motor and associative circuits or areas (Reviewed in44). In this sense, the expansion of the AP in parrots could resemble the expansion of the cortex in primates more closely than that of other clades of birds, like owls and waterfowl, where the expansion of the telencephalon is driven by the expansion of primary sensory areas26,27,45,46. It is currently not known if the expansion of the AP in parrots and corvids is related to particular circuits or all of them, but there is little evidence that parrots or songbirds have expanded visual, auditory and/or somatosensory areas of the AP39,46,47, suggesting that the expansion of the AP in parrots and corvids may be more associated with the expansion of associative areas, like the caudolateral nidopallium (NCL).

The concomitant expansion of SpM and the telencephalon in parrots suggest that like in mammals, the evolution of complex cognitive abilities is linked with an increase in the connectivity between the telencephalon and cerebellum. As mentioned before (see introduction), it is widely recognized in mammals that the circuits that connect the telencephalon with the cerebellum are important for complex cognitive abilities, but in birds all attention so far has concentrated almost exclusively on the telencephalon and no consideration has given to how extra-telencephalic circuits may contribute to the cognitive abilities of parrots and other birds.

In birds most studies focus on the NCL as the substrate for complex cognitive abilities3,48. NCL is considered the closest avian equivalent of the mammalian prefrontal cortex, based on hodological, electrophysiological, functional, and neurochemical evidence (reviewed in49). In primates, trans-synaptic tracing has shown direct connections between the prefrontal cortex and the cerebellum10,50 (Fig. 1). In birds, comparable trans-synaptic tracing has yet to be done, but traditional tracing studies strongly suggest that the AP, including NCL, connects with the cerebellum through SpM. As mentioned before, the arcopallium projects to SpM and receives projections from both the mesopallium and the nidopallium44. Wild and Farabaugh51 showed that in the zebra finch (Taeniopygia guttata), the lateral part of the intermediate arcopallium receives projections directly from the frontal part of the nidopallium and NCL, and this same area sends dense projections to the lateral SpM (Fig. 1). Interestingly, these same authors do not report any projections of this same area of the arcopallium to the PL, which other authors21 have reported from more general injections in the arcopallium of the pigeon. Thus, the projections from the arcopallium to SpM and PL arise from different populations of arcopallial cells and SpM appears to be the only relay between the NCL and the cerebellum. The lack of expansion of PL in parrots (Figs 3B,D and S1) supports this contention.

It is thought that the capacity of complex cognitive abilities in primates and some birds like parrots and corvids is related to the ability to generate mental representations of objects thus allowing the mental manipulation of these objects and the prediction of possible outcomes52. Through their extensive connections with sensory and premotor areas, the mammalian PFC and avian NCL are thought to perform executive control over these mental models in accordance with internal goals53. At the same time, the cerebellum encodes internal models that reproduce the crucial properties of mental representations in the cerebral cortex10,54,55. Then, connections from the PFC to the cerebellum allow the cerebellum to update these internal models if incongruencies are detected between the internal model and self-generated goals52,55. Our results showing a differential expansion of SpM in parrots suggest strongly that, as in mammals, the interaction of mental representations originated in the telencephalon with internal models from the cerebellum are also crucial for complex cognitive abilities in birds. However, this is accomplished through an alternative circuit that does not exists in mammals. It is not clear to what extent the NCL/Arcopallium-SpM-cerebellum pathway and the PFC-pons-cerebellum converge in terms of connectivity and physiology. In primates, and particularly humans, there is an expansion of the specific areas of the cerebellar hemispheres that receive projections from the PFC14,56. SpM sends projections from folia VI to VIII20,57,58, but these folia are not especially large in parrots59.

Another factor that is likely to contribute to the exceptional expansion of SpM in parrots, but not other birds, is the number and density of neurons. Relative to body size, parrots and songbirds have more neurons than other birds, and their neuronal densities exceed those found in mammals, especially in the pallium, the avian homologue of the cortex36. Although songbirds (including corvids) and parrots have similar neuronal numbers and densities in the pallium, there are also differences between these two groups. In examining the data provided in Olkowicz et al.36, we found that as the brain increases in absolute size, the pallium of parrots gains neurons with respect to the cerebellum at a higher rate than passerines and other birds (Fig. 4). In other words, parrots have a significantly higher ratio of pallial to cerebellar neurons than songbirds and other birds (parrots, 1.6: songbirds, 0.98: other birds, 0.7). Note that this is also different than mammals in two significant aspects. First, the ratio between pallial and cerebellar neurons in mammals is constant across groups; even though primates have much higher neuronal densities than other mammals60, the cerebellum and the pallium gain cells proportionate to each other across mammals. Second, this ratio is much lower in mammals than in birds (0.26 in mammals).

Functions of SpM Expansion

The expansion of SpM that is unique to parrots (Fig. 2 and Table S3) may be key to the complex sensorimotor coordination and planning that is require for the extractive foraging that most species of parrots use for feeding. Most parrots feed on hard-shelled fruits and seeds. This requires a lot of fine manipulation to extract the nutritious contents from inside the fruit/seed. Usually, manipulation of these food items is achieved by coordination of a secure grasp of the objects with the foot, a muscular tongue and highly curved beak61,62,63. In mammals, several studies have highlighted the importance of sensorimotor cortico-cerebellar circuits in the fine control of voluntary movements e.g.64, but also in sensorimotor prediction65. SpM is well suited for these tasks as, like the pontine nuclei of mammals, SpM receives projections from sensory, motor and premotor areas of the telencephalon of birds (Fig. 1). This includes the putative homologues of the visual, somatosensory and motor cortex of birds22,23,66,67 as well as the aforementioned connections with NCL51,68,69. The expansion of SpM may not only be crucial for the execution of complex foraging behavior of parrots but also the learning of complex motor skills. In mammals, cortico-cerebellar pathways are involved in the learning of complex motor behaviors, such as tool use e.g.70, and several studies suggest that parrots are only able to perform complex extractions after learning by observation of conspecifics71,72. The expansion of SpM may also be important for other behaviors which parrots are capable of and that demand the capacity for planning, execution and understanding complex behavioural sequences, such as the string pulling task73 and the use of tools e.g.74. Finally, it is possible that the enlargement of SpM in parrots is also important in the performance of complex social play behavior. Parrots are one of the few groups of birds that exhibit social play, along with corvids and hornbills75. Recently, Kerney et al.76, found a correlation between the size of the main components of cortico-cerebellar systems in primates and the amount of play behaviors exhibited. The expansion of SpM in parrots suggests the same could be true for birds.

Conclusions and Considerations

Our results suggest that parrots’ brains may be unique among birds in having an expanded nucleus that connects the associative pallium with the cerebellum: the SpM. This suggests that, as in primates, telencephalon-cerebellar pathways play a major role in controlling complex behaviors. A major caveat in our understanding of the function of telencephalon-cerebellar pathways in birds is the lack of detailed information of the connections and organizations of these neural circuits in birds. For example, in mammals, an important component of cortico-cerebellar pathways are feedback projections from the cerebellum to the cortex via the cerebellar nuclei and the thalamus (see Fig. 1)10. This creates two loops between the cortex and the cerebellum: a motor loop and a prefrontal loop. It is unclear if birds (or other vertebrates) have homologs of the cerebellar hemispheres and the dentate nucleus, which gives rise to the cerebellar projections to the thalamus in mammals34,77. Instead, the lateral cerebellar nucleus of birds, which is thought to be homologous to the interposed nuclei of mammals34, sends projections to the dorsal thalamus, which then projects to either the rostral Wulst67,78, the putative homologue of the motor cortex in birds, or NCL (Fig. 1)68. This at least suggests the existence of both a motor and a prefrontal telencephalon-cerebellar loop in birds. Regardless of the specifics of these poorly understood pathways, our results clearly implicate SpM as a key brain region in the evolution of complex cognitive abilities in birds and provide a unique opportunity to reveal convergent characteristics of these circuits.