Behavior Selection Controlled by a Dopaminergic-Inhibitory Neural Circuit

Time:2016-01-22

  In a article published online in NEURON on January 22, entitled "Visual Cue-Discriminative Dopaminergic Control of Visuomotor Transformation and Behavior Selection",  Dr. DU Jiulin's lab at the Institute of Neuroscience, Chinese Academy of Sciences, identified a novel circuit mechanism through which behavior selection is controlled at the stage of visuomotor transformation by a visually responsive dopaminergic-inhibitory neural module.

  Appropriate behavioral responses to ever-changing visual cues in the natural environment is critical for animals' well-being and survival. The generation of visual behavior engages visual pathways and downstream motor pathways. Although the generation of different visually evoked behaviors certainly involves signal processing along visual pathways, many of animals' actions are selected at the visuomotor transformation stage, where visual information is transformed into motor commands. This selective visuomotor transformation filters out superfluous information and permits relevant visual signals to trigger appropriate behaviors. However, due to the complexity of neural circuits involved in visuomotor transformation, how the transformation process is controlled for the selection of appropriate behaviors in a visual stimulus-specific manner remains poorly understood.

  To investigate the neural mechanism underlying differential behavior selection, Dr. DU's group firstly established a behavior selection model in zebrafish larvae. They found that zebrafish larvae showed escape behavior in response to threatening but not non-threatening visual stimuli. This stimulus-specific control is executed at the stage of visuomotor transformation. To identify the controlling neural circuit, Dr. DU's group combined electrophysiological, pharmacological, genetic, optogenetic and behavioral methods and found that dopaminergic neurons in the caudal hypothalamic and glycinergic interneurons in the hindbrain constitute a neural module to control visual information transmission from the visual center to the motor command neuron. To dissect how this neural module specifically allows threatening stimuli to evoke escape behavior, Dr. DU's  group performed in vivo calcium imaging and electrophysiological recording on hypothalamic dopaminergic neurons and hindbrain glycinergic interneurons and found that the control specificity is achieved by the differential visual responsiveness of the dopaminergic-inhibitory module. Both types of neurons are activated by non-threatening stimuli, imposing an enhanced inhibition to visual information transmission. By contrast, threatening stimuli suppress these neurons' activities, leading to dis-inhibition of visual information transmission and generation of escape behavior.

  Together, these results identify a visually responsive dopaminergic-inhibitory circuit module that controls visuomotor transformation and behavior selection in a stimulus-specific manner. It is the first identification of a neural circuit mechanism underlying behavior selection in vertebrates at synaptic, circuit to behavioral levels. The behavioral relevance-dependent control mechanism uncovered in this work expands our knowledge of sensorimotor transformation control and further reinforces the importance of neuromodulation in behavior selection. Furthermore, the sensory stimulus-responsive property of neuromodulatory neurons may represent a general mechanism through which neuromodulation can be tuned by sensory cues to help animals generate appropriate behavior in a natural environment.

  This work was carried out by YAO Yuanyuan, LI Xiaoquan, ZHANG Baibing and collaborators under the supervision of Dr. DU Jiulin at Institute of Neuroscience, Chinese Academy of Sciences, in collaboration with Dr. ZENG Shaoqun's group at the Wuhan National Laboratory for Optoelectronics, Huazhong University of Science and Technology. It was supported by grants of the Strategic Priority Research Program from Chinese Academy of Sciences, "973" Programs from Ministry of Science and Technology of China, Natural Science Foundation of China, Shanghai Subject Chief Scientist Program and Young Scientist Program from the Science and Technology Commission of Shanghai.

  

  Figure legend: Hypothalamic dopaminergic neurons and hindbrain glycinergic interneurons control visual information transmission from the optic tectum to the escape circuit in a stimulus-specific manner. In response to threatening stimuli, part of dopaminergic neurons and almost all of glycinergic interneurons decrease their activities, resulting in decreased inhibition of visual information transmission from the optic tectum to the escape circuit and generation of escape behavior. In response to non-threatening stimuli, part of dopaminergic neurons and almost all of glycinergic interneurons increase their activities, enhance inhibition of visual information transmission from the optic tectum to the escape circuit and prevent escape occurrence.

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