Using temperature to analyse temporal dynamics in the songbird motor pathway - PubMed (original) (raw)

Using temperature to analyse temporal dynamics in the songbird motor pathway

Michael A Long et al. Nature. 2008.

Abstract

Many complex behaviours, like speech or music, have a hierarchical organization with structure on many timescales, but it is not known how the brain controls the timing of behavioural sequences, or whether different circuits control different timescales of the behaviour. Here we address these issues by using temperature to manipulate the biophysical dynamics in different regions of the songbird forebrain involved in song production. We find that cooling the premotor nucleus HVC (formerly known as the high vocal centre) slows song speed across all timescales by up to 45 per cent but only slightly alters the acoustic structure, whereas cooling the downstream motor nucleus RA (robust nucleus of the arcopallium) has no observable effect on song timing. Our observations suggest that dynamics within HVC are involved in the control of song timing, perhaps through a chain-like organization. Local manipulation of brain temperature should be broadly applicable to the identification of neural circuitry that controls the timing of behavioural sequences and, more generally, to the study of the origin and role of oscillatory and other forms of brain dynamics in neural systems.

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Figures

Figure 1

Figure 1. Changes in HVC temperature affect song duration

a, Schematic showing the Peltier device and relevant parts of the song production pathway. b, Temperature measurement in HVC as a function of time after onset (open circle) of the indicated current through the Peltier device (heating, top; cooling, bottom); current offset is at closed circles. c, Calibration curves for brain temperature changes at various depths under the Peltier device (n = 4 birds). d, Representative sonograms (freq: 1kHz to 9kHz) recorded from Bird #3 with HVC heated (0.25A) and cooled (0.25A to 1.5A, 0.25A steps). At bottom, spectrogram of the control motif artificially stretched. e, Fractional change in duration (dilation) of song motif with temperature, relative to the pre-implantation song (n = 10 birds). The red symbols are from bird #3. f, Motif dilation averaged over all 10 birds. The shaded area represents the range over which the song stretch metric (%/°C) was calculated.

Figure 2

Figure 2. HVC cooling slows the song at all timescales

a , Dilation of subsyllabic structure versus HVC temperature change for all five syllables of bird #8. b, Dilation of syllable-onset intervals for the same bird. c, Dilation of motif-onset intervals for all 7 birds that produced concatenated motifs at all temperatures. d, Distribution of stretch metrics for the entire data set, including syllables (36 syllables, 8 birds,), syllable onsets (43 syllables, 9 birds,), and motif onsets (7 birds). Stretch of syllable-onset interval was strongly correlated with subsyllabic stretch (e) and motif-onset stretch (f) (for further details, see Supplementary Information).

Figure 3

Figure 3. Effects of RA temperature change on song timing

a, X-ray image of the implanted RA cooling device and approximate locations of HVC and RA. b, Temperature in RA (200 μm from cooling probe) and HVC as a function of RA probe current. Note that the RA probe produces some cooling in HVC. c, Change in motif duration as a function of RA probe current (n=4 birds, red squares show mean). d, Average change in motif duration (red squares) during RA probe cooling or heating, plotted as a function of HVC temperature. Also plotted is the average change in motif duration (blue circles) as a function of HVC temperature measured in the HVC cooling experiment (Fig 1f). e, Change in motif duration as a function of RA temperature, corrected for the effect of HVC temperature change. f, Stretchof subsyllabic elements for the population of RA cooled birds (n = 4 birds, 20 syllables), corrected for HVC temperature change.

Figure 4

Figure 4. Effects of RA temperature change on RA spiking activity

a, An example of the tonic spiking activity of an RA neuron in an anesthetized bird at various temperature changes. b, Average firing rate response (25 trials) to the application of 1A cooling current to the RA probe. c, Average tonic spiking rate versus temperature for all recorded neurons (19 cells, 7 birds). Filled red circles are from the example shown in (a). d, Spike train showing tonic spiking and spontaneous bursts (top). Incidence of bursts (defined as an instantaneous firing rate greater than 100 Hz) for all neurons (bottom).

Figure 5

Figure 5. Effect of unilateral HVC cooling on song timing. a

, Simultaneous temperature measurements from HVC in both hemispheres when the Peltier device was configured for right HVC cooling. b, Change in motif duration as a function of HVC temperature change during unilateral and bilateral cooling in bird #11. c, Spectrograms of song motif during control, bilateral, left and right HVC cooling. d, Selective dilation of subsyllabic element B, but not A, during left HVC cooling. e, Selective dilation of element A, but not B, during right HVC cooling. Dilation of subsyllabic element A (f) and B (g) during left (blue) and right (red) HVC cooling. h, Stretch metric of identified song segments during cooling of left, right, or both HVCs. Distributions of stretch nonuniformity values following bilateral (i) and unilateral (j) cooling. k, Nonuniformity values during left and right cooling show significant anticorrelation (p=0.026). Solid line shows the first principal component of the distribution.

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References

    1. Marder E, Bucher D. Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol. 2007;69:291–316. - PubMed
    1. Stent GS, et al. Neuronal generation of the leech swimming movement. Science. 1978;200:1348–57. - PubMed
    1. Williams H. Birdsong and singing behavior. Ann N Y Acad Sci. 2004;1016:1–30. - PubMed
    1. Konishi M. Birdsong: from behavior to neuron. Annu Rev Neurosci. 1985;8:125–70. - PubMed
    1. Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary, Serinus canarius. J Comp Neurol. 1976;165:457–86. - PubMed

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