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Using temperature to analyse temporal dynamics in the songbird motor pathway.

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.

SUBMITTER: Long MA

PROVIDER: S-EPMC2723166 | biostudies-literature | 2008 Nov

REPOSITORIES: biostudies-literature

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Using temperature to analyse temporal dynamics in the songbird motor pathway.

Long Michael A MA Fee Michale S MS

Nature 20081101 7219

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 a ...[more]

PMID: 19005546

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Project description:Different neuronal types within brain motor areas contribute to the generation of complex motor behaviors. A widely studied songbird forebrain nucleus (HVC) has been recognized as fundamental in shaping the precise timing characteristics of birdsong. This is based, among other evidence, on the stretching and the "breaking" of song structure when HVC is cooled. However, little is known about the temperature effects that take place in its neurons. To address this, we investigated the dynamics of HVC both experimentally and computationally. We developed a technique where simultaneous electrophysiological recordings were performed during temperature manipulation of HVC. We recorded spontaneous activity and found three effects: widening of the spike shape, decrease of the firing rate and change in the interspike interval distribution. All these effects could be explained with a detailed conductance based model of all the neurons present in HVC. Temperature dependence of the ionic channel time constants explained the first effect, while the second was based in the changes of the maximal conductance using single synaptic excitatory inputs. The last phenomenon, only emerged after introducing a more realistic synaptic input to the inhibitory interneurons. Two timescales were present in the interspike distributions. The behavior of one timescale was reproduced with different input balances received form the excitatory neurons, whereas the other, which disappears with cooling, could not be found assuming poissonian synaptic inputs. Furthermore, the computational model shows that the bursting of the excitatory neurons arises naturally at normal brain temperature and that they have an intrinsic delay at low temperatures. The same effect occurs at single synapses, which may explain song stretching. These findings shed light on the temperature dependence of neuronal dynamics and present a comprehensive framework to study neuronal connectivity. This study, which is based on intrinsic neuronal characteristics, may help to understand emergent behavioral changes.

Project description:Key pointsVentrolateral thalamus (VL) integrates information from cerebellar nuclei and motor cortical layer VI. Inputs from the cerebellar nuclei evoke large-amplitude responses that depress upon repetitive stimulation while layer VI inputs from motor cortex induce small-amplitude facilitating responses. We report that the spiking of VL neurons can be determined by the thalamic membrane potential, the frequency of cerebellar inputs and the duration of pauses after cerebellar high frequency stimulation. Inputs from motor cortical layer VI shift the VL membrane potential and modulate the VL spike output in response to cerebellar stimulation. These results help us to decipher how the cerebellar output is integrated in VL and modulated by motor cortical input.AbstractOrchestrating complex movements requires well-timed interaction of cerebellar, thalamic and cerebral structures, but the mechanisms underlying the integration of cerebro-cerebellar information in motor thalamus remain largely unknown. Here we investigated how excitatory inputs from cerebellar nuclei (CN) and primary motor cortex layer VI (M1-L6) neurons may regulate the activity of neurons in the mouse ventrolateral (VL) thalamus. Using dual-optical stimulation of the CN and M1-L6 axons and in vitro whole-cell recordings of the responses in VL neurons, we studied the individual responses as well as the effects of combined CN and M1-L6 stimulation. Whereas CN inputs evoked large-amplitude responses that were depressed upon repetitive stimulation, M1-L6 inputs elicited small-amplitude responses that were facilitated upon repetitive stimulation. Moreover, pauses in CN stimuli could directly affect VL spiking probability, an effect that was modulated by VL membrane potential. When CN and M1-L6 pathways were co-activated, motor cortical afferents increased the thalamic spike output in response to cerebellar stimulation, indicating that CN and M1 synergistically, yet differentially, control the membrane potential and spiking pattern of VL neurons.

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Using temperature to analyse temporal dynamics in the songbird motor pathway.

Publications

Using temperature to analyse temporal dynamics in the songbird motor pathway.

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