Learning: The cerebellum influences vocal timing

We are starting to understand how the cerebellum contributes to vocal learning in songbirds.
  1. Court Hull  Is a corresponding author
  1. Duke University, United States

Spoken language is a fundamental human skill that relies on vocal learning. Many species are able to produce vocalizations, but only a small number are considered vocal learners. For example, humans learn to speak by imitating the speech of others, and juvenile passerine songbirds learn to sing by mimicking adult birds (Bolhuis et al., 2010).

In both humans and songbirds, the brain circuits essential for vocal learning connect the cortex (a highly evolved brain structure involved in associative learning) and the basal ganglia (a more evolutionarily ancient brain region involved in reinforcement learning; Brainard and Doupe, 2013; Mooney, 2009). In humans, another part of the brain, called the cerebellum or ‘little brain’, may also have an important role in vocal learning. This region is highly active during speech, and children with cerebellar dysfunction often take much longer to learn how to speak (Ziegler and Ackermann, 2017). Moreover, patients with cerebellar disease or damage often suffer from ‘ataxic dysarthria’, a motor speech disorder that affects the timing and clarity of speech (Ackermann, 2008). A better knowledge of how cerebellar circuits interact with the basal ganglia and the cortex is thus critical for understanding how vocal learning is established, and how it is disrupted by injury or disease.

Birds are commonly used to study vocal learning, but the role of the cerebellum in birdsong has so far been unclear. Now, in eLife, Ludivine Pidoux and colleagues at Paris Descartes University report that this structure is also essential for the timing aspects of vocal learning in zebra finches (Pidoux et al., 2018).

Studies in humans and non-human primates have shown that the cerebellum contributes to motor control and motor learning through several pathways. In addition to descending pathways to the spinal cord, the cerebellum connects to the cortex and the basal ganglia via the thalamus, a central structure that relays motor and sensory signals to and from the cortex (Strick et al., 2009; Bostan and Strick, 2018). Since an anatomical connection between the cerebellum and the basal ganglia is also present in songbirds, it was important to test whether the cerebellum could influence the activity of basal ganglia and participate in song learning (Person et al., 2008).

Using a series of elegant anatomical, electrophysiological and pharmacological approaches, Pidoux et al. demonstrate for the first time that this cerebellar pathway has an important role in vocal learning in birds. Stimulating a cluster of neurons in the cerebellum known as the dentate nucleus, activated neurons that participate in song learning within the basal ganglia (Area X) via the thalamus (Figure 1). This activity also propagated via the thalamus to various areas in the cortex, including certain motor areas controlling the vocal chords.

Brain circuits for vocal learning in songbirds and humans.

Songbird circuits that support vocal learning (left), also labeled according to their homologous structures in humans (right). These include the cortex (gray and dark gray), the basal ganglia (Area X/BG; red) and the thalamus (green and light green). Pidoux et al. have revealed a functional connection (bold arrows) from an area in the cerebellum, the dentate nucleus (DN; blue), through the dorsal thalamic zone in the thalamus (DTZ; green) to Area X (red) in the basal ganglia. Abbreviations: DLM medial portion of the dorsolateral nucleus of the anterior thalamus; HVC song-related motor nuclei, used as proper name; LMAN lateral magnocellular nucleus of the anterior nidopallium; RA robust nucleus of the arcopallium.

This pathway appears to be the only route for the dentate nucleus to modulate the basal ganglia. When the activity was blocked in thedorsal thalamic zone connecting the cerebellum and Area X, neurons in the basal ganglia were prevented from responding to stimulation in the cerebellum. In contrast, blocking the pathways connecting the cortex with Area X did not affect the activity of this region. These results suggest that the cerebellum can influence the circuits in the basal ganglia required for vocal learning, implying that it could play a key role in this process.

Indeed, when this cerebellar pathway was disrupted, juvenile birds were less able to copy the songs of adults. This manipulation particularly affected aspects of song timing. However, this was not the case when the same pathway was disrupted in adult birds, suggesting that the cerebellum is specifically relevant for learning key aspects of song timing. This is consistent with the well-known role of the cerebellum in learned motor timing (Ivry and Spencer, 2004; Mauk et al., 2000). Together, these results provide a complete functional circuit pathway from the cerebellum to the basal ganglia to the premotor neurons involved in song production.

By identifying the specific role of the cerebellum and its circuits in regulating how the timing of a song is learned, Pidoux et al. have shed new light on the neural basis of vocal learning. However, we are only starting to understand how the cerebellum contributes to vocal learning. Next, we need to discover exactly how this brain region shapes the timing of the learned songs. Meanwhile, the ‘little brain’ must be recognized as a key player in the network of circuits that enable vocal learning.


Article and author information

Author details

  1. Court Hull

    Court Hull is in the Department of Neurobiology, Duke University, Durham, United States

    For correspondence
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0360-8367

Publication history

  1. Version of Record published: August 28, 2018 (version 1)


© 2018, Hull

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.


  • 1,767
  • 173
  • 2

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Court Hull
Learning: The cerebellum influences vocal timing
eLife 7:e40447.

Further reading

    1. Neuroscience
    Salima Messaoudi, Ada Allam ... Isabelle Caille
    Research Article

    The fragile X syndrome (FXS) represents the most prevalent form of inherited intellectual disability and is the first monogenic cause of autism spectrum disorder. FXS results from the absence of the RNA-binding protein FMRP (fragile X messenger ribonucleoprotein). Neuronal migration is an essential step of brain development allowing displacement of neurons from their germinal niches to their final integration site. The precise role of FMRP in neuronal migration remains largely unexplored. Using live imaging of postnatal rostral migratory stream (RMS) neurons in Fmr1-null mice, we observed that the absence of FMRP leads to delayed neuronal migration and altered trajectory, associated with defects of centrosomal movement. RNA-interference-induced knockdown of Fmr1 shows that these migratory defects are cell-autonomous. Notably, the primary Fmrp mRNA target implicated in these migratory defects is microtubule-associated protein 1B (MAP1B). Knocking down MAP1B expression effectively rescued most of the observed migratory defects. Finally, we elucidate the molecular mechanisms at play by demonstrating that the absence of FMRP induces defects in the cage of microtubules surrounding the nucleus of migrating neurons, which is rescued by MAP1B knockdown. Our findings reveal a novel neurodevelopmental role for FMRP in collaboration with MAP1B, jointly orchestrating neuronal migration by influencing the microtubular cytoskeleton.

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Maximilian Nagel, Marco Niestroj ... Marc Spehr
    Research Article

    In most mammals, conspecific chemosensory communication relies on semiochemical release within complex bodily secretions and subsequent stimulus detection by the vomeronasal organ (VNO). Urine, a rich source of ethologically relevant chemosignals, conveys detailed information about sex, social hierarchy, health, and reproductive state, which becomes accessible to a conspecific via vomeronasal sampling. So far, however, numerous aspects of social chemosignaling along the vomeronasal pathway remain unclear. Moreover, since virtually all research on vomeronasal physiology is based on secretions derived from inbred laboratory mice, it remains uncertain whether such stimuli provide a true representation of potentially more relevant cues found in the wild. Here, we combine a robust low-noise VNO activity assay with comparative molecular profiling of sex- and strain-specific mouse urine samples from two inbred laboratory strains as well as from wild mice. With comprehensive molecular portraits of these secretions, VNO activity analysis now enables us to (i) assess whether and, if so, how much sex/strain-selective ‘raw’ chemical information in urine is accessible via vomeronasal sampling; (ii) identify which chemicals exhibit sufficient discriminatory power to signal an animal’s sex, strain, or both; (iii) determine the extent to which wild mouse secretions are unique; and (iv) analyze whether vomeronasal response profiles differ between strains. We report both sex- and, in particular, strain-selective VNO representations of chemical information. Within the urinary ‘secretome’, both volatile compounds and proteins exhibit sufficient discriminative power to provide sex- and strain-specific molecular fingerprints. While total protein amount is substantially enriched in male urine, females secrete a larger variety at overall comparatively low concentrations. Surprisingly, the molecular spectrum of wild mouse urine does not dramatically exceed that of inbred strains. Finally, vomeronasal response profiles differ between C57BL/6 and BALB/c animals, with particularly disparate representations of female semiochemicals.