Avian neurons consume three times less glucose than mammalian neurons.

Brains are among the most energetically costly tissues in the mammalian body.1 This is predominantly caused by expensive neurons with high glucose demands.2 Across mammals, the neuronal energy budget appears to be fixed, possibly posing an evolutionary constraint on brain growth.3-6 Compared to similarly sized mammals, birds have higher numbers of neurons, and this advantage conceivably contributes to their cognitive prowess.7 We set out to determine the neuronal energy budget of birds to elucidate how they can metabolically support such high numbers of neurons. We estimated glucose metabolism using positron emission tomography (PET) and 2-[18F]fluoro-2-deoxyglucose ([18F]FDG) as the radiotracer in awake and anesthetized pigeons. Combined with kinetic modeling, this is the gold standard to quantify cerebral metabolic rate of glucose consumption (CMRglc).8 We found that neural tissue in the pigeon consumes 27.29 ± 1.57 µmol glucose per 100 g per min in an awake state, which translates into a surprisingly low neuronal energy budget of 1.86 × 10-9 ± 0.2 × 10-9 µmol glucose per neuron per minute. This is approximately 3 times lower than the rate in the average mammalian neuron.3 The remarkably low neuronal energy budget explains how pigeons, and possibly other avian species, can support such high numbers of neurons without associated metabolic costs or compromising neuronal signaling. The advantage in neuronal processing of information at a higher efficiency possibly emerged during the distinct evolution of the avian brain.

Morphology of the "prefrontal" nidopallium caudolaterale in the long-distance night-migratory Eurasian blackcap (Sylvia atricapilla).

Migrating birds have developed remarkable navigational capabilities to successfully master biannual journeys between their breeding and wintering grounds. To reach their intended destination, they need to calculate navigational goals from a large variety of natural directional and positional cues to set a meaningful motor output command. One brain area, which has been associated with such executive functions, is the nidopallium caudolaterale (NCL), which, due to its striking similarities in terms of neurochemistry, connectivity and function, is considered analogous to the mammalian prefrontal cortex. To establish a baseline for further analyses elucidating the neuronal correlates underlying avian navigation, we performed quantitative and qualitative analyses of dopaminergic fibres in the brains of long-distance night-migratory Eurasian blackcaps (Sylvia atricapilla). We identified four regions in the caudal telencephalon, each of which was characterized by its specific dopaminergic innervation pattern. At least three of them presumably constitute subareas of the NCL in Eurasian blackcaps and could thus be involved in integrating navigational input from different sensory systems. The observed heterogeneity and parcellation of the NCL subcompartments in this migratory species could be a consequence of the special demands related to navigation.

Avian pallial circuits and cognition: A comparison to mammals.

Cognitive functions are similar in birds and mammals. So, are therefore pallial cellular circuits and neuronal computations also alike? In search of answers, we move in from bird's pallial connectomes, to cortex-like sensory canonical circuits and connections, to forebrain micro-circuitries and finally to the avian "prefrontal" area. This voyage from macro- to micro-scale networks and areas reveals that both birds and mammals evolved similar neural and computational properties in either convergent or parallel manner, based upon circuitries inherited from common ancestry. Thus, these two vertebrate classes evolved separately within 315 million years with highly similar pallial architectures that produce comparable cognitive functions.

A comparative analysis of the dopaminergic innervation of the executive caudal nidopallium in pigeon, chicken, zebra finch, and carrion crow.

Despite the long, separate evolutionary history of birds and mammals, both lineages developed a rich behavioral repertoire of remarkably similar executive control generated by distinctly different brains. The seat for executive functioning in birds is the nidopallium caudolaterale (NCL) and the mammalian equivalent is known as the prefrontal cortex (PFC). Both are densely innervated by dopaminergic fibers, and are an integration center of sensory input and motor output. Whereas the variation of the PFC has been well documented in different mammalian orders, we know very little about the NCL across the avian clade. In order to investigate whether this structure adheres to species-specific variations, this study aimed to describe the trajectory of the NCL in pigeon, chicken, carrion crow and zebra finch. We employed immunohistochemistry to map dopaminergic innervation, and executed a Gallyas stain to visualize the dorsal arcopallial tract that runs between the NCL and the arcopallium. Our analysis showed that whereas the trajectory of the NCL in the chicken is highly comparable to the pigeon, the two Passeriformes show a strikingly different pattern. In both carrion crow and zebra finch, we identified four different subareas of high dopaminergic innervation that span the entire caudal forebrain. Based on their sensory input, motor output, and involvement in dopamine-related cognitive control of the delineated areas here, we propose that at least three morphologically different subareas constitute the NCL in these songbirds. Thus, our study shows that comparable to the PFC in mammals, the NCL in birds varies considerably across species.

Nuclear organization and morphology of catecholaminergic neurons and certain pallial terminal networks in the brain of the Nile crocodile, Crocodylus niloticus.

In the current study, we use tyrosine hydroxylase (TH) immunohistochemistry to detail the nuclear parcellation and cellular morphology of neurons belonging to the catecholaminergic system in the brain of the Nile crocodile. In general, our results are similar to that found in another crocodilian (the spectacled caiman) and indeed other vertebrates, but certain differences of both evolutionary and functional significance were noted. TH immunopositive (TH+) neurons forming distinct nuclei were observed in the olfactory bulb (A16), hypothalamus (A11, A13-15), midbrain (A8-A10), pons (A5-A7) and medulla oblongata (area postrema, C1, C2, A1, A2), encompassing the more commonly observed nuclear complexes of this system across vertebrates. In addition, TH + neurons forming distinct nuclei not commonly identified in vertebrates were observed in the anterior olfactory nucleus, the pretectal nuclear complex, adjacent to the posterior commissure, and within nucleus laminaris, nucleus magnocellularis lateralis and the lateral vestibular nucleus. Palely stained TH + neurons were observed in some of the serotonergic nuclei, including the medial and lateral divisions of the superior raphe nucleus and the inferior raphe and inferior reticular nucleus, but not in other serotonergic nuclei. In birds, a high density of TH + fibres and pericellular baskets in the dorsal ventricular ridge marks the location of the nidopallium caudolaterale (NCL), a putative avian analogue of mammalian prefrontal cortex. In the dorsal ventricular ridge (DVR) of the crocodile a small region in the caudolateral anterior DVR (ADVRcl) revealed a slightly higher density of TH + fibres and some pericellular baskets (formed by only few TH + fibres). These results are discussed in an evolutionary and functional framework.

fMRI Reveals a Novel Region for Evaluating Acoustic Information for Mate Choice in a Female Songbird.

Selection of sexual partners is among the most critical decisions that individuals make and is therefore strongly shaped by evolution. In social species, where communication signals can convey substantial information about the identity, state, or quality of the signaler, accurate interpretation of communication signals for mate choice is crucial. Despite the importance of social information processing, to date, relatively little is known about the neurobiological mechanisms that contribute to sexual decision making and preferences. In this study, we used a combination of whole-brain functional magnetic resonance imaging (fMRI), immediate early gene expression, and behavior tests to identify the circuits that are important for the perception and evaluation of courtship songs in a female songbird, the zebra finch (Taeniopygia guttata). Female zebra finches are sensitive to subtle differences in male song performance and strongly prefer the longer, faster, and more stereotyped courtship songs to non-courtship renditions. Using BOLD fMRI and EGR1 expression assays, we uncovered a novel region involved in auditory perceptual decision making located in a sensory integrative region of the avian central nidopallium outside the traditionally studied auditory forebrain pathways. Changes in activity in this region in response to acoustically similar but categorically divergent stimuli showed stronger parallels to behavioral responses than an auditory sensory region. These data highlight a potential role for the caudocentral nidopallium (NCC) as a novel node in the avian circuitry underlying the evaluation of acoustic signals and their use in mate choice.