Abstract

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.

Highlights

  • Coordinated motor behaviors require a delicate sequence of gestures

  • It is believed that it is highly responsible for generating the precise timing of songs, and this has been tested by manipulating it with temperature

  • We built a computational model with a detailed description of ion channel conductances and temperature dependency

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Summary

Introduction

Coordinated motor behaviors require a delicate sequence of gestures Their precise timing depends on instructions coming from motor control areas in the brain. A widely used model to study complex behavior is birdsong, which consists of a succession of highly stereotyped vocal gestures. Like humans with their speech, oscine birds that account for approximately forty percent of the known species, need to learn their vocalizations from a tutor [1,2,3,4,5]. The well characterized set of forebrain nuclei in charge of this task is called the “song system” [6,7,8]. It has proven to be a valuable model to study the network properties necessary to generate the precise motor patterns of song [9,10,11,12]

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