Dataset Information

Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch.

ABSTRACT: The thalamostriatal system is a major network in the mammalian brain, originating principally from the intralaminar nuclei of thalamus. Its functions remain unclear, but a subset of these projections provides a pathway through which the cerebellum communicates with the basal ganglia. Both the cerebellum and basal ganglia play crucial roles in motor control. Although songbirds have yielded key insights into the neural basis of vocal learning, it is unknown whether a thalamostriatal system exists in the songbird brain. Thalamic nucleus DLM is an important part of the song system, the network of nuclei required for learning and producing song. DLM receives output from song system basal ganglia nucleus Area X and sits within dorsal thalamus, the proposed avian homolog of the mammalian intralaminar nuclei that also receives projections from the cerebellar nuclei. Using a viral vector that specifically labels presynaptic axon segments, we show in Bengalese finches that dorsal thalamus projects to Area X, the basal ganglia nucleus of the song system, and to surrounding medial striatum. To identify the sources of thalamic input to Area X, we map DLM and cerebellar-recipient dorsal thalamus (DTCbN ). Surprisingly, we find both DLM and dorsal anterior DTCbN adjacent to DLM project to Area X. In contrast, the ventral medial subregion of DTCbN projects to medial striatum outside Area X. Our results suggest the basal ganglia in the song system, like the mammalian basal ganglia, integrate feedback from the thalamic region to which they project as well as thalamic regions that receive cerebellar output.

SUBMITTER: Nicholson DA

PROVIDER: S-EPMC5899675 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch.

Nicholson David A DA Roberts Todd F TF Sober Samuel J SJ

The Journal of comparative neurology 20180406 9

The thalamostriatal system is a major network in the mammalian brain, originating principally from the intralaminar nuclei of thalamus. Its functions remain unclear, but a subset of these projections provides a pathway through which the cerebellum communicates with the basal ganglia. Both the cerebellum and basal ganglia play crucial roles in motor control. Although songbirds have yielded key insights into the neural basis of vocal learning, it is unknown whether a thalamostriatal system exists ...[more]

PMID: 29520771

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Project description:To investigate mechanisms of action sequencing, we examined the relationship between timing and sequencing of syllables in Bengalese finch song. An individual's song comprises acoustically distinct syllables organized into probabilistic sequences: a given syllable potentially can transition to several different syllables (divergence points), and several different syllables can transition to a given syllable (convergence points). In agreement with previous studies, we found that more probable transitions at divergence points occur with shorter intersyllable gaps. One intuition for this relationship is that selection between syllables reflects a competitive branching process, in which stronger links to one syllable lead to both higher probabilities and shorter latencies for transitions to that syllable vs. competing alternatives. However, we found that simulations of competitive race models result in overlapping winning-time distributions for competing outcomes and fail to replicate the strong negative correlation between probability and gap duration found in song data. Further investigation of song structure revealed strong positive correlation between gap durations for transitions that share a common convergent point. Such transitions are not related by a common competitive process, but instead reflect a common terminal syllable. In contrast to gap durations, transition probabilities were not correlated at convergence points. Together, our data suggest that syllable selection happens early during the gap, with gap timing determined chiefly by the latency to syllable initiation. This may result from a process in which probabilistic sequencing is first stabilized, followed by a shortening of the latency to syllables that are sung more often.NEW & NOTEWORTHY Bengalese finch songs consist of probabilistic sequences of syllables. Previous studies revealed a strong negative correlation between transition probability and the duration of intersyllable gaps. We show here that the negative correlation is inconsistent with previous suggestions that timing at syllable transitions is governed by a race between competing alternatives. Rather, the data suggest that syllable selection happens early during the gap, with gap timing determined chiefly by the latency to syllable initiation.

Project description:BackgroundSinging in songbirds is a complex, learned behavior which shares many parallels with human speech. The avian vocal organ (syrinx) has two potential sound sources, and each sound generator is under unilateral, ipsilateral neural control. Different songbird species vary in their use of bilateral or unilateral phonation (lateralized sound production) and rapid switching between left and right sound generation (interhemispheric switching of motor control). Bengalese finches (Lonchura striata domestica) have received considerable attention, because they rapidly modify their song in response to manipulations of auditory feedback. However, how the left and right sides of the syrinx contribute to acoustic control of song has not been studied.MethodologyThree manipulations of lateralized syringeal control of sound production were conducted. First, unilateral syringeal muscular control was eliminated by resection of the left or right tracheosyringeal portion of the hypoglossal nerve, which provides neuromuscular innervation of the syrinx. Spectral and temporal features of song were compared before and after lateralized nerve injury. In a second experiment, either the left or right sound source was devoiced to confirm the role of each sound generator in the control of acoustic phonology. Third, air pressure was recorded before and after unilateral denervation to enable quantification of acoustic change within individual syllables following lateralized nerve resection.SignificanceThese experiments demonstrate that the left sound source produces louder, higher frequency, lower entropy sounds, and the right sound generator produces lower amplitude, lower frequency, higher entropy sounds. The bilateral division of labor is complex and the frequency specialization is the opposite pattern observed in most songbirds. Further, there is evidence for rapid interhemispheric switching during song production. Lateralized control of song production in Bengalese finches may enhance acoustic complexity of song and facilitate the rapid modification of sound production following manipulations of auditory feedback.

Project description:BACKGROUND:The proteins of avian eggshell organic matrices are thought to control the mineralization of the eggshell in the shell gland (uterus). Proteomic analysis of such matrices identified many candidates for such a role. However, all matrices analyzed to date come from species of one avian family, the Phasianidae. To analyze the conservation of such proteins throughout the entire class Aves and to possibly identify a common protein toolkit enabling eggshell mineralization, it is important to analyze eggshell matrices from other avian families. Because mass spectrometry-based in-depth proteomic analysis still depends on sequence databases as comprehensive and accurate as possible, the obvious choice for a first such comparative study was the eggshell matrix of zebra finch, the genome sequence of which is the only songbird genome published to date. RESULTS:The zebra finch eggshell matrix comprised 475 accepted protein identifications. Most of these proteins (84 %) were previously identified in species of the Phasianidae family (chicken, turkey, quail). This also included most of the so-called eggshell-specific proteins, the ovocleidins and ovocalyxins. Ovocleidin-116 was the second most abundant protein in the zebra finch eggshell matrix. Major proteins also included ovocalyxin-32 and -36. The sequence of ovocleidin-17 was not contained in the sequence database, but a presumptive homolog was tentatively identified by N-terminal sequence analysis of a prominent 17 kDa band. The major proteins also included three proteins similar to ovalbumin, the most abundant of which was identified as ovalbumin with the aid of two characteristic phosphorylation sites. Several other proteins identified in Phasianidae eggshell matrices were not identified. When the zebra finch sequence database contained a sequence similar to a missing phasianid protein it may be assumed that the protein is missing from the matrix. This applied to ovocalyxin-21/gastrokine-1, a major protein of the chicken eggshell matrix, to EDIL3 and to lactadherin. In other cases failure to identify a particular protein may be due to the absence of this protein from the sequence database, highlighting the importance of better, more comprehensive sequence databases. CONCLUSIONS:The results indicate that ovocleidin-116, ovocleidin-17, ovocalyxin-36 and ovocalyxin-32 may be universal avian eggshell-mineralizing proteins. All the more important it is to elucidate the role of these proteins at the molecular level. This cannot be achieved by proteomic studies but will need application of other methods, such as atomic force microscopy or gene knockouts. However, it will also be important to analyze more eggshell matrices of different avian families to unequivocally identify other mineralization toolkit proteins apart from ovocleidins and ovocalyxins. Progress in this respect will depend critically on the availability of more, and more comprehensive, sequence databases. The development of faster and cheaper nucleotide sequencing methods has considerably accelerated genome and transcriptome sequencing, but this seems to concur with frequent publication of incomplete and fragmented sequence databases.

Dataset Information

Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch.

Publications

Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch.

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