Optogenetic perturbations reveal the dynamics of an oculomotor integrator

Optogenetic perturbations reveal the dynamics of an oculomotor integrator
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DOI:
10.3389/fncir.2014.00010
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发表时间:
2014-02-28
影响因子:
3.5
通讯作者:
Machens, Christian K.
Machens, Christian K.
中科院分区:
医学3区
文献类型:
--
作者:
Goncalves, Pedro J.;Arrenberg, Aristides B.;Machens, Christian K.

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许多神经系统可以在持续放电的神经元中存储短期信息。这种持续的活动被认为是通过神经元之间的反复反馈来维持的。这一假设已针对动眼神经积分器 (OI) 进行了详细充实,所谓的“线吸引器”网络模型可以解释大量的观察结果。在这里,我们表明存在大量这样的模型,通过反复兴奋和抑制的相对强度来区分。在每个模型中,神经元的放电率向持续活动状态放松。然而,放松的动态可能有很大不同,并且取决于反复兴奋和抑制的水平。为了确定正确的模型,我们通过对表达盐视紫红质或通道视紫红质的斑马鱼的 OI 进行光遗传学扰动来直接测量这些松弛动态。我们发现,OI 的瞬时抑制性刺激会导致刺激同侧持续向心的眼睛位置变化。兴奋性刺激同样会引起向心眼位置变化,但仅发生在刺激的对侧。这些结果表明,OI 的动力学是围绕中心吸引子状态(眼睛的零位置)组织的,该中心吸引子状态可以稳定系统免受随机扰动。我们的结果对系统的电路连接提出了新的限制,并为持久活动背后的机制提供了新的见解。
Many neural systems can store short-term information in persistently firing neurons. Such persistent activity is believed to be maintained by recurrent feedback among neurons. This hypothesis has been fleshed out in detail for the oculomotor integrator (OI) for which the so-called "line attractor" network model can explain a large set of observations. Here we show that there is a plethora of such models, distinguished by the relative strength of recurrent excitation and inhibition. In each model, the firing rates of the neurons relax toward the persistent activity states. The dynamics of relaxation can be quite different, however, and depend on the levels of recurrent excitation and inhibition. To identify the correct model, we directly measure these relaxation dynamics by performing optogenetic perturbations in the OI of zebrafish expressing halorhodopsin or channelrhodopsin. We show that instantaneous, inhibitory stimulations of the OI lead to persistent, centripetal eye position changes ipsilateral to the stimulation. Excitatory stimulations similarly cause centripetal eye position changes, yet only contralateral to the stimulation. These results show that the dynamics of the OI are organized around a central attractor state the null position of the eyes which stabilizes the system against random perturbations. Our results pose new constraints on the circuit connectivity of the system and provide new insights into the mechanisms underlying persistent activity.