Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron

Summary: Visual neurons that track objects on a collision course are often finely tuned to their target stimuli because this is critical for survival. The presynaptic neural networks converging on these neurons and their role in tuning them remain poorly understood. We took advantage of well-known c...

Full description

Bibliographic Details
Main Authors: Ying Zhu, Richard B. Dewell, Hongxia Wang, Fabrizio Gabbiani
Format: Article
Language:English
Published: Elsevier 2018-05-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124718306387
id doaj-d4422234be81414f85eb39610382d5a0
record_format Article
spelling doaj-d4422234be81414f85eb39610382d5a02020-11-24T21:33:41ZengElsevierCell Reports2211-12472018-05-0123823652378Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection NeuronYing Zhu0Richard B. Dewell1Hongxia Wang2Fabrizio Gabbiani3Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA; Quantitative and Computational Biosciences Graduate Program, Baylor College of Medicine, Houston, TX 77030, USADepartment of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USADepartment of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USADepartment of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA; Quantitative and Computational Biosciences Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA; Electrical and Computer Engineering Department, Rice University, Houston, TX 77005, USA; Corresponding authorSummary: Visual neurons that track objects on a collision course are often finely tuned to their target stimuli because this is critical for survival. The presynaptic neural networks converging on these neurons and their role in tuning them remain poorly understood. We took advantage of well-known characteristics of one such neuron in the grasshopper visual system to investigate the properties of its presynaptic input network. We find the structure more complex than hitherto realized. In addition to dynamic lateral inhibition used to filter out background motion, presynaptic circuits include normalizing inhibition and excitatory interactions mediated by muscarinic acetylcholine receptors. These interactions preferentially boost responses to coherently expanding visual stimuli generated by colliding objects, as opposed to spatially incoherent controls, helping to discriminate between them. Hence, in addition to active dendritic conductances within collision-detecting neurons, multiple layers of inhibitory and excitatory presynaptic connections are needed to finely tune neural circuits for collision detection. : In the locust visual system, Zhu et al. study the presynaptic circuitry of a collision-detecting neuron. They characterize local excitatory connections mediated by muscarinic acetylcholine receptors tuning the neuron to coherently expanding visual stimuli. Additionally, they describe a global inhibitory mechanism normalizing the excitatory inputs the cell receives. Keywords: LGMD, DCMD, collision avoidance, lateral excitation, looming, divisive normalization, muscarine, scopolaminehttp://www.sciencedirect.com/science/article/pii/S2211124718306387
collection DOAJ
language English
format Article
sources DOAJ
author Ying Zhu
Richard B. Dewell
Hongxia Wang
Fabrizio Gabbiani
spellingShingle Ying Zhu
Richard B. Dewell
Hongxia Wang
Fabrizio Gabbiani
Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron
Cell Reports
author_facet Ying Zhu
Richard B. Dewell
Hongxia Wang
Fabrizio Gabbiani
author_sort Ying Zhu
title Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron
title_short Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron
title_full Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron
title_fullStr Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron
title_full_unstemmed Pre-synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision-Detection Neuron
title_sort pre-synaptic muscarinic excitation enhances the discrimination of looming stimuli in a collision-detection neuron
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2018-05-01
description Summary: Visual neurons that track objects on a collision course are often finely tuned to their target stimuli because this is critical for survival. The presynaptic neural networks converging on these neurons and their role in tuning them remain poorly understood. We took advantage of well-known characteristics of one such neuron in the grasshopper visual system to investigate the properties of its presynaptic input network. We find the structure more complex than hitherto realized. In addition to dynamic lateral inhibition used to filter out background motion, presynaptic circuits include normalizing inhibition and excitatory interactions mediated by muscarinic acetylcholine receptors. These interactions preferentially boost responses to coherently expanding visual stimuli generated by colliding objects, as opposed to spatially incoherent controls, helping to discriminate between them. Hence, in addition to active dendritic conductances within collision-detecting neurons, multiple layers of inhibitory and excitatory presynaptic connections are needed to finely tune neural circuits for collision detection. : In the locust visual system, Zhu et al. study the presynaptic circuitry of a collision-detecting neuron. They characterize local excitatory connections mediated by muscarinic acetylcholine receptors tuning the neuron to coherently expanding visual stimuli. Additionally, they describe a global inhibitory mechanism normalizing the excitatory inputs the cell receives. Keywords: LGMD, DCMD, collision avoidance, lateral excitation, looming, divisive normalization, muscarine, scopolamine
url http://www.sciencedirect.com/science/article/pii/S2211124718306387
work_keys_str_mv AT yingzhu presynapticmuscarinicexcitationenhancesthediscriminationofloomingstimuliinacollisiondetectionneuron
AT richardbdewell presynapticmuscarinicexcitationenhancesthediscriminationofloomingstimuliinacollisiondetectionneuron
AT hongxiawang presynapticmuscarinicexcitationenhancesthediscriminationofloomingstimuliinacollisiondetectionneuron
AT fabriziogabbiani presynapticmuscarinicexcitationenhancesthediscriminationofloomingstimuliinacollisiondetectionneuron
_version_ 1725952482039824384