Neural Mechanisms of Cognitive Control and Emotion in Birds

In the present Research Topic, we have been successful in attracting contributions from a wide range of research centers around the globe. The new results gathered in a variety of biological disciplines represent important advances toward a better understanding of emotion and cognitive control in birds. Out of 21 articles by 67 authors (2 brief original research reports, 15 original research reports, and four review articles including one systematic review study), 10 studies focused on galliform precocial birds (and their hatchlings), nine on passerine birds (songbirds including crows and Java sparrows), and two on pigeons. By reviewing these studies, we hope to provide an update on cutting edge results hallmarking knowledge on avian brain and behaviors of today. We are grateful for the contributors, the guest editors and the reviewers for their efforts and intriguing ideas, which, so we believe, will set the foundation for future progress in avian physiology in a highly comprehensive manner, ranging across the fields of behavioral, anatomical, endocrinological, biochemical and evolutionary biology.

Animals are under continuous and endless barrages of stressors both from ambient physical world and social life. Kato et al. reports their novel finding on the molecular basis of stress responses and specified neurosecretory protein GL/GM (NPGL/NPGM), which acts as the stress mediator in the mediobasal hypothalamus. In particular, social isolation stress causes an acute increase in the expression of these proteins. Pross et al. examined the extended amygdala (division of the dorsal striatum) and found multiple types of enkephalin cells involved in stress regulation. Detailed neurochemical identification of the limbic network will constitute the critical basis for physiological specification of stress responses. Comparisons of songbirds (zebra finches ZFs and Bengalese finches BFs) led Kim et al. to suggest that spontaneous singing (undirected songs, United States) could be associated with environmental stress. These two species of finches revealed striking differences in the frequency of “dark singing,” where BFs emit United States much more than ZFs. Ambient light condition critically controls the singing motivation, but with a strong species difference.

Rich lines of evidence and ideas seem to converge on the positive emotional aspects of singing. Singh and Iyenga reviewed the opioid receptors in songbird brain and suggested that birds regulate singing and song learning by intrinsic motivational control. In accordance, the review by Riters et al. suggests that the nucleus accumbens in the medial striatum could be the site for intrinsic reward system that enables birds to proactively seek for mate. Kim and Kojima in their second paper, presented endocannabinoids as the activators of undirected spontaneous singing in songbirds. Study of singing behavior does not only tackle the issues of learned vocalization, but also those of its emotional/motivational background.

Lateralized hemispheric control is widely observed in sensory perception, cognition, and executive control of behaviors. Protti-Sánchez et al. reports a unique case where the umami-tastes (tasting of amino acids) yield lateralized activation in the chick limbic nucleus taeniae. Xiao and Güntürkün further expand the scope toward an associative cortex, or “prefrontal”-like avian analogue, the nidopallium caudolaterale (NCL) of pigeons. They stress the importance of sequential build-up of lateralization through the cascade of signal processing in the visual system. The detailed study on transmitter receptors in NCL by Herold et al. should also be referred to in the light of functional lateralization. Readers of the subject often feel lost in the plethora of literature, unable to construct the framework for understanding these issues. The systematic review article by Soma provides us with such a framework, i.e., a comprehensive survey of visual lateralization. In particular, the finding of opposite lateralization patterns in passerine and non-passerine birds strikingly underlines the importance of evolutionary perspectives.

Studies of filial imprinting are still actively progressing. Aoki et al. propose a novel and quantitative method of imprinting that allows partial constraint of the body and head in awake chicks. Meparishvili et al. pointed out tyrosine kinase (Src) as a novel key player in innate predisposition and engram formation in the pallial network of domestic chicks. It is also noted that the kinase system plays a critical role in execution of social behaviors of adults, just as Moaraf et al. revealed the involvement of GSK-3β in the social behaviors of zebra finches; its inhibition caused birds to move closer to a stranger than to a familiar companion, furthermore, the treated birds showed hyperactivity. The cellular target of the thyroid hormone, another player critically involved in the sensitive period, was examined by Saheki et al., who revealed that the hormone acutely enhances GABA-AR mediated synaptic inhibition, supporting the idea that the excitation-inhibition balance is critical for the control of critical period.

Beside function, morphology of the avian brain is also subject to developmental control. Stingo-Hirmas et al. give us a unique example where the size of cerebellum could be a predictor of the habituation to fearful objects in adult chickens. Also, the importance of careful behavioral testing and control of genetic background are being stressed in this study. One should not overlook the importance of descriptive studies such as detailed information on gene expression either. The avian hippocampus has been assumed to lack distinct subdivisions and layer structures. Fujita et al. present a significant contribution to our understanding of the avian hippocampus by detailed in situ hybridization analysis of serotonin receptor subtypes. In another paper, Fujita et al. were successful in the morphological dissociation between the dorsal and medial raphe in the chick brainstem by the same set of serotonin receptor subfamilies. Acute behavioral pharmacology in quails by Pichová et al. clearly showed functional control of reward expectation by the dopamine system. Notably, the manipulation of D1 and D2 receptors by antagonists yielded coherent rather than opposite results, meaning that both receptor types are likely involved in the given aspects of reward prediction.

Several new and powerful techniques have been applied to unravel the confounding issues of emotional control. Pendergraft et al. applied FDG-PET imaging of the brain in awake crows, and revealed that the activation of the nucleus taeniae amygdala (limbic) and nidopallium caudolaterale (NCL, medial portion) requires multimodal combination of multimodal stimuli of conspecifics, namely the sight of food and the sound of conspecific vocalization during foraging. Similarly innovative approach was successfully applied in the study of event-related mismatch responses reported in Java sparrows by Mori and Okanoya. Field potentials recorded from the auditory area of telencephalon (NCM) revealed significant effects of deviations from the repeated/habituated sounds in both pure tone and natural vocalization. Furthermore, the same team Fujii et al. contributes a comprehensive review on the question of why females are so choosy about male songs. As with all other biological disciplines, physiological mechanisms should be studied in the light of evolution/adaptive values, because evolutional thinking is a rich source of novel approaches in physiology.

All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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