Heterogeneous organization and connectivity of the chicken auditory thalamus (<i>Gallus gallus</i>)

Wang, Yuan; Zorio, Diego A. R.; Karten, Harvey J.

doi:10.1002/cne.24262

Cited by 11 publications

(17 citation statements)

References 62 publications

(138 reference statements)

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“…Comparable to the pigeon, the putative chicken NCL is a multimodal integration center that is organized in a similar dorsolateral to ventromedial fashion of sensory modalities (Martin Metzger, Jiang, & Braun, ; Metzger et al, ). The dorsal medial NCL is the main recipient of auditory information as targeted by afferents from field L1/L3 and the shell region of Ov (Wang, Zorio, & Karten, ). The center region of the putative NCL receives visual information from Ep and caudal division of HA, and somatosensory input is relayed via the rostral part of HA.…”

Section: Discussionmentioning

confidence: 99%

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

Eugen

Tabrik

Güntürkün

et al. 2020

J of Comparative Neurology

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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.

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Section: Discussionmentioning

confidence: 99%

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

Eugen

Tabrik

Güntürkün

et al. 2020

J of Comparative Neurology

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“…The thalamus (dorsal thalamus) contains numerous CCK-expressing neurons in mammals (Voigt and Uhl 1988;Young 1988, 1989a;De Belleroche et al 1990;Senatorov et al 1997;Giacobini and Wray 2008) and birds (Lowell and Mello 2011; Wang et al 2017). In mammals, CCK cells of the auditory thalamus and cerebral cortex are reciprocally connected and might be involved in seizure genesis (Senatorov et al 1997).…”

Section: Thalamusmentioning

confidence: 99%

Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems

et al. 2019

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Cholecystokinin (CCK) is a neuropeptide that modulates processes such as digestion, satiety and anxiety. CCK-type peptides have been characterized in jawed vertebrates and invertebrates, but little is known about CCK-type signalling in the most ancient group of vertebrates, the agnathans. Here we have cloned and sequenced a cDNA encoding a sea lamprey (Petromyzon marinus L.) CCK-type precursor (PmCCK), which contains a CCK-type octapeptide sequence (PmCCK-8) that is highly similar to gnathostome CCKs. Using mRNA in situ hybridization, the distribution of PmCCK-expressing neurons was mapped in the CNS of P. marinus. This revealed PmCCK-expressing neurons in the hypothalamus, posterior tubercle, prethalamus, nucleus of the medial longitudinal fasciculus, midbrain tegmentum, isthmus, rhombencephalic reticular formation and the putative nucleus of the solitary tract. Some PmCCK-expressing neuronal populations were only observed in adults, revealing 3 important differences with larvae. We generated an antiserum to PmCCK-8 to enable immunohistochemical analysis of CCK expression, which revealed that GABA or glutamate, but not serotonin, tyrosine hydroxylase or neuropeptide Y, are co-expressed in some PmCCK-8-immunoreactive (ir) neurons. Importantly, this is the first demonstration of co-localization of GABA and CCK in neurons of a non-mammalian vertebrate. We also characterized extensive cholecystokinergic fibre systems of the CNS, including innervation of habenular subnuclei. A conspicuous PmCCK-8-ir tract ascending in the lateral rhombencephalon selectively innervates a glutamatergic population in the dorsal isthmic grey. Interestingly, this tract is reminiscent of the secondary gustatory/visceral tract of teleosts. In conclusion, this study provides important new information on the evolution of the cholecystokinergic system in vertebrates.

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“…As both in chicken and mice AP-2δ is expressed in homologous regions during development and disruption of the Tcfap2 d in mice led to an ablation of the IC, future efforts could be directed towards generating AP-2δ knockout chicken germlines that possibly develop selective lesions of the auditory midbrain. The layout of the chicken midbrain is very well known, and the visual and auditory processing networks have been delineated in great detail (Luksch, 2003 ; Wylie et al, 2009 ; Wang et al, 2017 ; Lischka et al, 2018a ). This could open up tremendous opportunities for network analysis and understanding of multimodal integration in the midbrain.…”

Section: Discussionmentioning

confidence: 99%

“…While the differentiation of the IC subdivision was not the focus of this analysis, it should be noted that there is an ongoing discussion on the subdivisions of the IC in birds, a discussion that might profit from a thorough analysis of AP-2δ expression (Puelles et al, 1994;Wang and Karten, 2010;Niederleitner and Luksch, 2012). This is even more relevant as, starting at E16, parts of the intercollicular zone medial to the IC (Wang et al, 2017) were also expressing AP-2δ. At embryonic day 18, the labeling intensity in the IC decreased and the AP-2δ signal at E20 was almost absent, indicating that the expression window of AP-2δ has closed.…”

Section: Ap-2δ Expression During Chicken Developmentmentioning

confidence: 99%

AP-2δ Expression Kinetics in Multimodal Networks in the Developing Chicken Midbrain

Kettler

Sid

Schaub

et al. 2021

Front. Neural Circuits

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AP-2 is a family of transcription factors involved in many aspects of development, cell differentiation, and regulation of cell growth and death. AP-2δ is a member of this group and specific gene expression patterns are required in the adult mouse brain for the development of parts of the inferior colliculus (IC), as well as the cortex, dorsal thalamus, and superior colliculus. The midbrain is one of the central areas in the brain where multimodal integration, i.e., integration of information from different senses, occurs. Previous data showed that AP-2δ-deficient mice are viable but due to increased apoptosis at the end of embryogenesis, lack part of the posterior midbrain. Despite the absence of the IC in AP-2δ-deficient mice, these animals retain at least some higher auditory functions. Neuronal responses to tones in the neocortex suggest an alternative auditory pathway that bypasses the IC. While sufficient data are available in mammals, little is known about AP-2δ in chickens, an avian model for the localization of sounds and the development of auditory circuits in the brain. Here, we identified and localized AP-2δ expression in the chicken midbrain during embryogenesis. Our data confirmed the presence of AP-2δ in the inferior colliculus and optic tectum (TeO), specifically in shepherd’s crook neurons, which are an essential component of the midbrain isthmic network and involved in multimodal integration. AP-2δ expression in the chicken midbrain may be related to the integration of both auditory and visual afferents in these neurons. In the future, these insights may allow for a more detailed study of circuitry and computational rules of auditory and multimodal networks.

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Heterogeneous organization and connectivity of the chicken auditory thalamus (Gallus gallus)

Cited by 11 publications

References 62 publications

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

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

Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems

AP-2δ Expression Kinetics in Multimodal Networks in the Developing Chicken Midbrain

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