Showing papers by "Michale S. Fee published in 2011"

Changes in the neural control of a complex motor sequence during learning

Abstract: The acquisition of complex motor sequences often proceeds through trial-and-error learning, requiring the deliberate exploration of motor actions and the concomitant evaluation of the resulting performance. Songbirds learn their song in this manner, producing highly variable vocalizations as juveniles. As the song improves, vocal variability is gradually reduced until it is all but eliminated in adult birds. In the present study we examine how the motor program underlying such a complex motor behavior evolves during learning by recording from the robust nucleus of the arcopallium (RA), a motor cortex analog brain region. In young birds, neurons in RA exhibited highly variable firing patterns that throughout development became more precise, sparse, and bursty. We further explored how the developing motor program in RA is shaped by its two main inputs: LMAN, the output nucleus of a basal ganglia-forebrain circuit, and HVC, a premotor nucleus. Pharmacological inactivation of LMAN during singing made the song-aligned firing patterns of RA neurons adultlike in their stereotypy without dramatically affecting the spike statistics or the overall firing patterns. Removing the input from HVC, on the other hand, resulted in a complete loss of stereotypy of both the song and the underlying motor program. Thus our results show that a basal ganglia-forebrain circuit drives motor exploration required for trial-and-error learning by adding variability to the developing motor program. As learning proceeds and the motor circuits mature, the relative contribution of LMAN is reduced, allowing the premotor input from HVC to drive an increasingly stereotyped song.

Vocal babbling in songbirds requires the basal ganglia-recipient motor thalamus but not the basal ganglia.

Abstract: Young songbirds produce vocal “babbling,” and the variability of their songs is thought to underlie a process of trial-and-error vocal learning. It is known that this exploratory variability requires the “cortical” component of a basal ganglia (BG) thalamocortical loop, but less understood is the role of the BG and thalamic components in this behavior. We found that large bilateral lesions to the songbird BG homolog Area X had little or no effect on song variability during vocal babbling. In contrast, lesions to the BG-recipient thalamic nucleus DLM (medial portion of the dorsolateral thalamus) largely abolished normal vocal babbling in young birds and caused a dramatic increase in song stereotypy. These findings support the idea that the motor thalamus plays a key role in the expression of exploratory juvenile behaviors during learning.

Control of Vocal and Respiratory Patterns in Birdsong: Dissection of Forebrain and Brainstem Mechanisms Using Temperature

Abstract: Learned motor behaviors require descending forebrain control to be coordinated with midbrain and brainstem motor systems In songbirds, such as the zebra finch, regular breathing is controlled by brainstem centers, but when the adult songbird begins to sing, its breathing becomes tightly coordinated with forebrain-controlled vocalizations The periods of silence (gaps) between song syllables are typically filled with brief breaths, allowing the bird to sing uninterrupted for many seconds While substantial progress has been made in identifying the brain areas and pathways involved in vocal and respiratory control, it is not understood how respiratory and vocal control is coordinated by forebrain motor circuits Here we combine a recently developed technique for localized brain cooling, together with recordings of thoracic air sac pressure, to examine the role of cortical premotor nucleus HVC (proper name) in respiratory-vocal coordination We found that HVC cooling, in addition to slowing all song timescales as previously reported, also increased the duration of expiratory pulses (EPs) and inspiratory pulses (IPs) Expiratory pulses, like song syllables, were stretched uniformly by HVC cooling, but most inspiratory pulses exhibited non-uniform stretch of pressure waveform such that the majority of stretch occurred late in the IP Indeed, some IPs appeared to change duration by the earlier or later truncation of an underlying inspiratory event These findings are consistent with the idea that during singing the temporal structure of EPs is under the direct control of forebrain circuits, whereas that of IPs can be strongly influenced by circuits downstream of HVC, likely in the brainstem An analysis of the temporal jitter of respiratory and vocal structure suggests that IPs may be initiated by HVC at the end of each syllable and terminated by HVC immediately before the onset of the next syllable

Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds

Abstract: Accurate timing is a critical aspect of motor control, yet the temporal structure of many mature behaviors emerges during learning from highly variable exploratory actions. How does a developing brain acquire the precise control of timing in behavioral sequences? To investigate the development of timing, we analyzed the songs of young juvenile zebra finches. These highly variable vocalizations, akin to human babbling, gradually develop into temporally stereotyped adult songs. We find that the durations of syllables and silences in juvenile singing are formed by a mixture of two distinct modes of timing: a random mode producing broadly distributed durations early in development, and a stereotyped mode underlying the gradual emergence of stereotyped durations. Using lesions, inactivations, and localized brain cooling, we investigated the roles of neural dynamics within two premotor cortical areas in the production of these temporal modes. We find that LMAN (lateral magnocellular nucleus of the nidopallium) is required specifically for the generation of the random mode of timing and that mild cooling of LMAN causes an increase in the durations produced by this mode. On the contrary, HVC (used as a proper name) is required specifically for producing the stereotyped mode of timing, and its cooling causes a slowing of all stereotyped components. These results show that two neural pathways contribute to the timing of juvenile songs and suggest an interesting organization in the forebrain, whereby different brain areas are specialized for the production of distinct forms of neural dynamics.

Learning to breathe and sing: development of respiratory-vocal coordination in young songbirds.

Abstract: How do animals with learned vocalizations coordinate vocal production with respiration? Songbirds such as the zebra finch learn their songs, beginning with highly variable babbling vocalizations known as subsong. After several weeks of practice, zebra finches are able to produce a precisely timed pattern of syllables and silences, precisely coordinated with expiratory and inspiratory pulses (Franz M, Goller F. J Neurobiol 51: 129–141, 2002). While respiration in adult song is well described, relatively little is known about respiratory patterns in subsong or about the processes by which respiratory and vocal patterns become coordinated. To address these questions, we recorded thoracic air sac pressure in juvenile zebra finches prior to the appearance of any consistent temporal or acoustic structure in their songs. We found that subsong contains brief inspiratory pulses (50 ms) alternating with longer pulses of sustained expiratory pressure (50–500 ms). In striking contrast to adult song, expiratory pulses often contained multiple (0–8) variably timed syllables separated by expiratory gaps and were only partially vocalized. During development, expiratory pulses became shorter and more stereotyped in duration with shorter and fewer nonvocalized parts. These developmental changes eventually resulted in the production of a single syllable per expiratory pulse and a single inspiratory pulse filling each gap, forming a coordinated sequence similar to that of adult song. To examine the role of forebrain song-control nuclei in the development of respiratory patterns, we performed pressure recordings before and after lesions of nucleus HVC (proper name) and found that this manipulation reverses the developmental trends in measures of the respiratory pattern.

New methods for localizing and manipulating neuronal dynamics in behaving animals

Abstract: Where are the ‘prime movers’ that control behavior? Which circuits in the brain control the order in which individual motor gestures of a learned behavior are generated, and the speed at which they progress? Here we describe two techniques recently applied to localizing and characterizing the circuitry underlying the generation of vocal sequences in the songbird. The first utilizes small, localized, temperature changes in the brain to perturb the speed of neural dynamics. The second utilizes intracellular manipulation of membrane potential in the freely behaving animal to perturb the dynamics within a single neuron. Both of these techniques are broadly applicable in behaving animals to test hypotheses about the biophysical and circuit dynamics that allow neural circuits to march from one state to the next.

Vocal babbling in songbirds requires the basal ganglia-recipient motor

Abstract: Young songbirds produce vocal "babbling," and the variability of their songs is thought to underlie a process of trial-and-error vocal learning. It is known that this exploratory variability requires the "cortical" component of a basal ganglia (BG) thalamocortical loop, but less understood is the role of the BG and thalamic components in this behavior. We found that large bilateral lesions to the songbird BG homolog Area X had little or no effect on song variability during vocal babbling. In contrast, lesions to the BG-recipient thalamic nucleus DLM (medial portion of the dorsolateral thalamus) largely abolished normal vocal babbling in young birds and caused a dramatic increase in song stereotypy. These findings support the idea that the motor thalamus plays a key role in the expression of exploratory juvenile behaviors during learning.