Dataset Information

Rhythmic syllable-related activity in a songbird motor thalamic nucleus necessary for learned vocalizations.

ABSTRACT: Birdsong is a complex behavior that exhibits hierarchical organization. While the representation of singing behavior and its hierarchical organization has been studied in some detail in avian cortical premotor circuits, our understanding of the role of the thalamus in adult birdsong is incomplete. Using a combination of behavioral and electrophysiological studies, we seek to expand on earlier work showing that the thalamic nucleus Uvaeformis (Uva) is necessary for the production of stereotyped, adult song in zebra finch (Taeniopygia guttata). We confirm that complete bilateral lesions of Uva abolish singing in the 'directed' social context, but find that in the 'undirected' social context, such lesions result in highly variable vocalizations similar to early babbling song in juvenile birds. Recordings of neural activity in Uva reveal strong syllable-related modulation, maximally active prior to syllable onsets and minimally active prior to syllable offsets. Furthermore, both song and Uva activity exhibit a pronounced coherent modulation at 10Hz-a pattern observed in downstream premotor areas in adult and, even more prominently, in juvenile birds. These findings are broadly consistent with the idea that Uva is critical in the sequential activation of behavioral modules in HVC.

SUBMITTER: Danish HH

PROVIDER: S-EPMC5472270 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Rhythmic syllable-related activity in a songbird motor thalamic nucleus necessary for learned vocalizations.

Danish Husain H HH Aronov Dmitriy D Fee Michale S MS

PloS one 20170615 6

Birdsong is a complex behavior that exhibits hierarchical organization. While the representation of singing behavior and its hierarchical organization has been studied in some detail in avian cortical premotor circuits, our understanding of the role of the thalamus in adult birdsong is incomplete. Using a combination of behavioral and electrophysiological studies, we seek to expand on earlier work showing that the thalamic nucleus Uvaeformis (Uva) is necessary for the production of stereotyped, ...[more]

PMID: 28617829

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Project description:Rodents move rhythmically their facial whiskers and compute differences between signals predicted and those resulting from the movement to infer information about objects near their head. These computations are carried out by a large network of forebrain structures that includes the thalamus and the primary somatosensory (S1BF) and motor (M1wk) cortices. Spatially and temporally precise mechanorreceptive whisker information reaches the S1BF cortex via the ventroposterior medial thalamic nucleus (VPM). Other whisker-related information may reach both M1wk and S1BF via the axons from the posterior thalamic nucleus (Po). However, Po axons may convey, in addition to direct sensory signals, the dynamic output of computations between whisker signals and descending motor commands. It has been proposed that this input may be relevant for adjusting cortical responses to predicted vs. unpredicted whisker signals, but the effects of Po input on M1wk and S1BF function have not been directly tested or compared in vivo. Here, using electrophysiology, optogenetics and pharmacological tools, we compared in adult rats M1wk and S1BF in vivo responses in the whisker areas of the motor and primary somatosensory cortices to passive multi-whisker deflection, their dependence on Po activity, and their changes after a brief intense activation of Po axons. We report that the latencies of the first component of tactile-evoked local field potentials in M1wk and S1BF are similar. The evoked potentials decrease markedly in M1wk, but not in S1BF, by injection in Po of the GABAA agonist muscimol. A brief high-frequency electrical stimulation of Po decreases the responsivity of M1wk and S1BF cells to subsequent whisker stimulation. This effect is prevented by the local application of omega-agatoxin, suggesting that it may in part depend on GABA release by fast-spiking parvalbumin (PV)-expressing cortical interneurons. Local optogenetic activation of Po synapses in different cortical layers also diminishes M1wk and S1BF responses. This effect is most pronounced in the superficial layers of both areas, known to be the main source and target of their reciprocal cortico-cortical connections.

Project description:OBJECTIVE:Rhythmic brain stimulation has emerged as a powerful tool to modulate cognition and to target pathological oscillations related to neurological and psychiatric disorders. However, we lack a systematic understanding of how periodic stimulation interacts with endogenous neural activity as a function of the brain state and target. APPROACH:To address this critical issue, we applied periodic stimulation to a unified biophysical thalamic network model that generates multiple distinct oscillations, and examined thoroughly the impact of rhythmic stimulation on different oscillatory states. MAIN RESULTS:We found that rhythmic perturbation induces four basic response mechanisms: entrainment, acceleration, resonance and suppression. Importantly, the appearance and expression of these mechanisms depend highly on the intrinsic cellular dynamics in each state. Specifically, the low-threshold bursting of thalamocortical cells (TCs) in delta (?) oscillation renders the network relatively insensitive to entrainment; the high-threshold bursting of TCs in alpha (?) oscillation leads to widespread oscillation suppression while the tonic spiking of TC cells in gamma (?) oscillation results in prominent entrainment and resonance. In addition, we observed entrainment discontinuity during ? oscillation that is mediated by firing pattern switching of high-threshold bursting TC cells. Furthermore, we demonstrate that direct excitatory stimulation of the lateral geniculate nucleus (LGN) entrains thalamic oscillations via an asymmetric Arnold tongue that favors higher frequency entrainment and resonance, while stimulation of the inhibitory circuit, the reticular nucleus, induces much weaker and more symmetric entrainment and resonance. These results support the notion that rhythmic stimulation engages brain oscillations in a state- and target-dependent manner. SIGNIFICANCE:Overall, our study provides, for the first time, insights into how the biophysics of thalamic oscillations guide the emergence of complex, state-dependent mechanisms of target engagement, which can be leveraged for the future rational design of novel therapeutic stimulation modalities.

Dataset Information

Rhythmic syllable-related activity in a songbird motor thalamic nucleus necessary for learned vocalizations.

Publications

Rhythmic syllable-related activity in a songbird motor thalamic nucleus necessary for learned vocalizations.

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