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Neuron-specific cholinergic modulation of a forebrain song control nucleus.

ABSTRACT: Cholinergic activation profoundly affects vertebrate forebrain networks, but pathway, cell type, and modality specificity remain poorly understood. Here we investigated cell-specific cholinergic modulation of neurons in the zebra finch forebrain song control nucleus HVC using in vitro whole cell recordings. The HVC contains projection neurons that exclusively project to either another song motor nucleus RA (robust nucleus of the arcopallium) (HVC-RAn) or the basal ganglia Area X (HVC-Xn) and these populations are synaptically coupled by a network of GABAergic interneurons. Among HVC-RAn, we observed two physiologically distinct classes that fire either phasically or tonically to injected current. Muscarine excited phasic HVC-RAn and most HVC-Xn. Effects were observed under conditions of blockade of fast synaptic transmission and were reversed by atropine. In contrast, unlike what is commonly observed in mammalian systems, HVC interneurons were inhibited by muscarine and these effects were reversed by atropine. Thus cholinergic modulation reconfigures the HVC network in a more complex fashion than that implied by monolithic "gating." The two projection pathways are decoupled through suppression of the inhibitory network that links them, whereas each is simultaneously predominantly excited. We speculate that fluctuating cholinergic tone in HVC could modulate the interaction of song motor commands with basal ganglia circuitry associated with song perception and modification. Furthermore, if the in vitro distinction between RA-projecting neurons that we observed is also present in vivo, then the song system motor pathway exhibits greater physiological diversity than has been commonly assumed.

SUBMITTER: Shea SD

PROVIDER: S-EPMC2822690 | biostudies-literature | 2010 Feb

REPOSITORIES: biostudies-literature

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Neuron-specific cholinergic modulation of a forebrain song control nucleus.

Shea Stephen D SD Koch Henner H Baleckaitis Daniel D Ramirez Jan-Marino JM Margoliash Daniel D

Journal of neurophysiology 20091125 2

Cholinergic activation profoundly affects vertebrate forebrain networks, but pathway, cell type, and modality specificity remain poorly understood. Here we investigated cell-specific cholinergic modulation of neurons in the zebra finch forebrain song control nucleus HVC using in vitro whole cell recordings. The HVC contains projection neurons that exclusively project to either another song motor nucleus RA (robust nucleus of the arcopallium) (HVC-RAn) or the basal ganglia Area X (HVC-Xn) and the ...[more]

PMID: 19939956

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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.

Dataset Information

Neuron-specific cholinergic modulation of a forebrain song control nucleus.

Publications

Neuron-specific cholinergic modulation of a forebrain song control nucleus.

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