A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output

AbstractHow neural circuits drive behavior is a central question in neuroscience. Proper execution of motor behavior requires the precise coordination of many neurons. Within a motor circuit, individual neurons tend to play discrete roles by promoting or suppressing motor output. How exactly neurons function in specific roles to fine tune motor output is not well understood. In C. elegans, the interneuron RIM plays important yet complex roles in locomotion behavior. Here, we show that RIM both promotes and suppresses distinct features of locomotion behavior to fine tune motor output. This dual function is achieved via the excitation and inhibition of the same motor circuit by electrical and chemical neurotransmission, respectively. Additionally, this bi-directional regulation contributes to motor adaptation in animals placed in novel environments. Our findings reveal that individual neurons within a neural circuit may act in opposing ways to regulate circuit dynamics to fine tune behavioral output.

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Corollary discharge promotes a sustained motor state in a neural circuit for navigation

eLife ◽

10.7554/elife.68848 ◽

2021 ◽

Vol 10 ◽

Author(s):

Ni D Ji ◽

Vivek Venkatachalam ◽

Hillary Denise Rodgers ◽

Wesley Hung ◽

Taizo Kawano ◽

...

Keyword(s):

Sensory Processing ◽

Neural Circuit ◽

Genetic Manipulation ◽

Feedback Mechanism ◽

Corollary Discharge ◽

Neural Responses ◽

Motor Representation ◽

Motor Circuit ◽

C Elegans ◽

Positive Feedback Mechanism

Animals exhibit behavioral and neural responses that persist on longer time scales than transient or fluctuating stimulus inputs. Here, we report that C. elegans uses feedback from the motor circuit to a sensory processing interneuron to sustain its motor state during thermotactic navigation. By imaging circuit activity in behaving animals, we show that a principal postsynaptic partner of the AFD thermosensory neuron, the AIY interneuron, encodes both temperature and motor state information. By optogenetic and genetic manipulation of this circuit, we demonstrate that the motor state representation in AIY is a corollary discharge signal. RIM, an interneuron that is connected with premotor interneurons, is required for this corollary discharge. Ablation of RIM eliminates the motor representation in AIY, allows thermosensory representations to reach downstream premotor interneurons, and reduces the animal's ability to sustain forward movements during thermotaxis. We propose that feedback from the motor circuit to the sensory processing circuit underlies a positive feedback mechanism to generate persistent neural activity and sustained behavioral patterns in a sensorimotor transformation.

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Behavior in the Brain

Journal of Psychophysiology ◽

10.1027/0269-8803/a000016 ◽

2010 ◽

Vol 24 (2) ◽

pp. 76-82 ◽

Cited By ~ 15

Author(s):

Martin M. Monti ◽

Adrian M. Owen

Keyword(s):

Motor Behavior ◽

Functional Neuroimaging ◽

Brain Activity ◽

Motor Output ◽

The Unconscious ◽

Ethical Implications ◽

Brain Responses ◽

Minimally Conscious ◽

Brain Insults ◽

Brain Behavior

Recent evidence has suggested that functional neuroimaging may play a crucial role in assessing residual cognition and awareness in brain injury survivors. In particular, brain insults that compromise the patient’s ability to produce motor output may render standard clinical testing ineffective. Indeed, if patients were aware but unable to signal so via motor behavior, they would be impossible to distinguish, at the bedside, from vegetative patients. Considering the alarming rate with which minimally conscious patients are misdiagnosed as vegetative, and the severe medical, legal, and ethical implications of such decisions, novel tools are urgently required to complement current clinical-assessment protocols. Functional neuroimaging may be particularly suited to this aim by providing a window on brain function without requiring patients to produce any motor output. Specifically, the possibility of detecting signs of willful behavior by directly observing brain activity (i.e., “brain behavior”), rather than motoric output, allows this approach to reach beyond what is observable at the bedside with standard clinical assessments. In addition, several neuroimaging studies have already highlighted neuroimaging protocols that can distinguish automatic brain responses from willful brain activity, making it possible to employ willful brain activations as an index of awareness. Certainly, neuroimaging in patient populations faces some theoretical and experimental difficulties, but willful, task-dependent, brain activation may be the only way to discriminate the conscious, but immobile, patient from the unconscious one.

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PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C. elegans

Nature Neuroscience ◽

10.1038/nn.3253 ◽

2012 ◽

Vol 15 (12) ◽

pp. 1675-1682 ◽

Cited By ~ 68

Author(s):

Arantza Barrios ◽

Rajarshi Ghosh ◽

Chunhui Fang ◽

Scott W Emmons ◽

Maureen M Barr

Keyword(s):

Neural Circuit ◽

Searching Behavior ◽

Mate Searching ◽

C Elegans

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Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia

Journal of Applied Physiology ◽

10.1152/japplphysiol.00613.2002 ◽

2003 ◽

Vol 94 (6) ◽

pp. 2342-2349 ◽

Cited By ~ 107

Author(s):

Ying-Jie Peng ◽

Nanduri R. Prabhakar

Keyword(s):

Intermittent Hypoxia ◽

Motor Behavior ◽

Motor Output ◽

Chronic Intermittent Hypoxia ◽

Radical Scavenger ◽

Respiratory Behavior ◽

Cumulative Duration ◽

Posthypoxic Period ◽

Long Term Facilitation ◽

Sustained Hypoxia

Long-term facilitation (LTF) of breathing elicited by episodic hypoxia (EH) is an extensively studied example of plasticity of respiratory motor behavior. Previous studies employed the paradigm of EH wherein each episode of hypoxia was 5 min. This paradigm is rarely encountered in nature. Brief episodes of hypoxia are encountered frequently with recurrent apneas, wherein hypoxic episodes last a few seconds only. Recent studies suggest that chronic intermittent hypoxia (CIH) represents a form of oxidative stress involving reactive O2species. The objectives of the present study were to determine 1) whether acute, repeated, brief EH (15 s) elicit LTF in breathing and 2) whether prior conditioning with CIH modulates acute EH-induced LTF of breathing, and if so whether reactive O2 species are involved. Experiments were performed on anesthetized, vagotomized, paralyzed, and mechanically ventilated rats, and efferent phrenic nerve activity was monitored as an index of respiratory motor output. In control animals, acute EH (15-s hypoxia; 10 episodes; n = 9) increased minute neural respiration, which persisted during 60 min of the posthypoxic period, suggesting LTF of breathing. EH-induced LTF of respiration was markedly augmented in CIH-conditioned animals (15-s hypoxia, 9 episodes/h, 8 h/day for 10 days; n = 9). By contrast, conditioning with a comparable, cumulative duration of sustained hypoxia (4-h hypoxia; n = 8) did not augment LTF elicited by acute EH. Systemic administration of manganese (III) tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride (5 mg · kg−1 · day−1for 10 days), a potent scavenger of O[Formula: see text]·, prevented CIH-induced potentiation of LTF ( n = 9). These results demonstrate that 1) acute, brief EH elicits LTF in respiratory motor output; 2) prior conditioning with CIH, but not with comparable, cumulative duration of sustained hypoxia, augments LTF elicited by acute EH; and 3) O[Formula: see text]· radical scavenger prevents CIH-induced potentiation of LTF of respiration.

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Oscillatory integration windows in neurons

10.1101/081471 ◽

2016 ◽

Author(s):

Nitin Gupta ◽

Swikriti Saran Singh ◽

Mark Stopfer

Keyword(s):

Neural Circuits ◽

Neural Circuit ◽

Field Potential ◽

Coincidence Detection ◽

Uniform Structure ◽

Detection Mechanism ◽

Oscillation Frequencies ◽

Local Field Potential Lfp ◽

Oscillatory Cycle

AbstractOscillatory synchrony among neurons occurs in many species and brain areas, and has been proposed to help neural circuits process information. One hypothesis states that oscillatory input creates cyclic integration windows: specific times in each oscillatory cycle when postsynaptic neurons become especially responsive to inputs. With paired local field potential (LFP) and intracellular recordings and controlled stimulus manipulations we directly tested this idea in the locust olfactory system. We found that inputs arriving in Kenyon cells (KCs) sum most effectively in a preferred window of the oscillation cycle. With a computational model, we found that the non-uniform structure of noise in the membrane potential helps mediate this process. Further experiments performed in vivo demonstrated that integration windows can form in the absence of inhibition and at a broad range of oscillation frequencies. Our results reveal how a fundamental coincidence-detection mechanism in a neural circuit functions to decode temporally organized spiking.

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A genetic manipulation of motor neuron excitability does not alter locomotor output in Drosophila larvae

10.7287/peerj.preprints.469v1 ◽

2014 ◽

Author(s):

Erin C. McKiernan

Keyword(s):

Motor Neuron ◽

Motor Neurons ◽

Motor Behavior ◽

Genetic Manipulation ◽

Motor Output ◽

Membrane Properties ◽

Neuron Excitability ◽

Motor Neuron Excitability ◽

The Face

Motor activity, like that producing locomotion, is generated by networks of neurons. At the last output level of these networks are the motor neurons, which send signals to the muscles, causing them to contract. Current research in motor control is focused on finding out how motor neurons contribute to shaping the timing of motor behaviors. Are motor neurons just passive relayers of the signals they receive? Or, do motor neurons shape the signals before passing them on to the muscles, thereby influencing the timing of the behavior? It is now well accepted that motor neurons have active, intrinsic membrane properties - there are ion channels in the cell membrane that allow motor neurons to respond to input in non-linear and diverse ways. However, few direct tests of the role of motor neuron intrinsic properties in shaping motor behavior have been carried out, and many questions remain about the role of specific ion channel genes in motor neuron function. In this study, two potassium channel transgenes were expressed in Drosophila larvae, causing motor neurons to fire at lower levels of current stimulation and at higher frequencies, thereby increasing excitability. Mosaic animals were created in which some identified motor neurons expressed the transgenes while others did not. Motor output underlying crawling was compared in muscles innervated by control and experimental neurons in the same animals. Counterintuitively, no effect of the transgenic manipulation on motor output was seen. Future experiments are outlined to determine how the larval nervous system produces normal motor output in the face of altered motor neuron excitability.

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Prominent Inhibitory Projections Guide Sensorimotor Computation: An Invertebrate Perspective

10.20944/preprints201908.0112.v1 ◽

2019 ◽

Author(s):

Samantha Hughes ◽

Tansu Celikel

Keyword(s):

Motor Neurons ◽

Neural Circuits ◽

Neural Circuit ◽

Sensory Information ◽

Circuit Complexity ◽

Inhibitory Circuits ◽

Invertebrate Species ◽

Gating Mechanism ◽

Motor Actions ◽

Sensorimotor Representations

From single-cell organisms to complex neural networks, all evolved to provide control solutions to generate context and goal-specific actions. Neural circuits performing sensorimotor computation to drive navigation employ inhibitory control as a gating mechanism, as they hierarchically transform (multi)sensory information into motor actions. Here, we focus on this literature to critically discuss the proposition that prominent inhibitory projections form sensorimotor circuits. After reviewing the neural circuits of navigation across various invertebrate species, we argue that with increased neural circuit complexity and the emergence of parallel computations inhibitory circuits acquire new functions. The contribution of inhibitory neurotransmission for navigation goes beyond shaping the communication that drives motor neurons, instead, include encoding of emergent sensorimotor representations. A mechanistic understanding of the neural circuits performing sensorimotor computations in invertebrates will unravel the minimum circuit requirements driving adaptive navigation.

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Hikaru genki protein is secreted into synaptic clefts from an early stage of synapse formation in Drosophila

Development ◽

10.1242/dev.122.2.589 ◽

1996 ◽

Vol 122 (2) ◽

pp. 589-597 ◽

Cited By ~ 1

Author(s):

M. Hoshino ◽

E. Suzuki ◽

Y. Nabeshima ◽

C. Hama

Keyword(s):

Critical Period ◽

Synapse Formation ◽

Neural Circuits ◽

Motor Behavior ◽

Early Stage ◽

Axon Growth ◽

Number Of Factors ◽

Protein Functions ◽

Abnormal Motor ◽

Immunohistochemical Analyses

The development of neural circuits is regulated by a large number of factors that are localized at distinct neural sites. We report here the localization of one of these factors, hikaru genki (hig) protein, at synaptic clefts in the pupal and adult nervous systems of Drosophila. In hig mutants, unusually frequent bursting activity of the muscles and abnormal motor behavior during the adult stage suggest the misfunction of neuromuscular circuitry. Our immunohistochemical analyses revealed that hig protein, produced by neurons, is secreted from the presynaptic terminals into the spaces between the presynaptic and postsynaptic terminals. In addition, we have found that the localization of this protein in the synaptic spaces temporally correlates with its functional requirement during a critical period that occurs in the middle stage of pupal formation, a period when a number of dendrite and axon growth cones meet to form synapses. These findings indicate that hig protein functions in the formation of functional neural circuits from the early stages of synapse formation.

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Artificial Intelligence Based on Biological Neurons

Sensor Network Methodologies for Smart Applications - Advances in Information Security, Privacy, and Ethics ◽

10.4018/978-1-7998-4381-8.ch002 ◽

2020 ◽

pp. 25-53

Author(s):

Rinat Galiautdinov

Keyword(s):

Artificial Intelligence ◽

Neural Circuits ◽

Neural Circuit ◽

Next Generation ◽

New Approach ◽

Home Based

The chapter describes the new approach in artificial intelligence based on simulated biological neurons and creation of the neural circuits for the sphere of IoT which represent the next generation of artificial intelligence and IoT. Unlike existing technical devices for implementing a neuron based on classical nodes oriented to binary processing, the proposed path is based on simulation of biological neurons, creation of biologically close neural circuits where every device will implement the function of either a sensor or a “muscle” in the frame of the home-based live AI and IoT. The research demonstrates the developed nervous circuit constructor and its usage in building of the AI (neural circuit) for IoT.

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A novel device for real-time measurement and manipulation of licking behavior in head-fixed mice

Journal of Neurophysiology ◽

10.1152/jn.00500.2018 ◽

2018 ◽

Vol 120 (6) ◽

pp. 2975-2987 ◽

Cited By ~ 1

Author(s):

Brice Williams ◽

Anderson Speed ◽

Bilal Haider

Keyword(s):

Real Time ◽

Neural Activity ◽

Closed Loop ◽

Neural Circuits ◽

Neural Circuit ◽

Visual Behavior ◽

Sensory Stimuli ◽

Neural Recordings ◽

Control Signals ◽

Sensory Motor

The mouse has become an influential model system for investigating the mammalian nervous system. Technologies in mice enable recording and manipulation of neural circuits during tasks where they respond to sensory stimuli by licking for liquid rewards. Precise monitoring of licking during these tasks provides an accessible metric of sensory-motor processing, particularly when combined with simultaneous neural recordings. There are several challenges in designing and implementing lick detectors during head-fixed neurophysiological experiments in mice. First, mice are small, and licking behaviors are easily perturbed or biased by large sensors. Second, neural recordings during licking are highly sensitive to electrical contact artifacts. Third, submillisecond lick detection latencies are required to generate control signals that manipulate neural activity at appropriate time scales. Here we designed, characterized, and implemented a contactless dual-port device that precisely measures directional licking in head-fixed mice performing visual behavior. We first determined the optimal characteristics of our detector through design iteration and then quantified device performance under ideal conditions. We then tested performance during head-fixed mouse behavior with simultaneous neural recordings in vivo. We finally demonstrate our device’s ability to detect directional licks and generate appropriate control signals in real time to rapidly suppress licking behavior via closed-loop inhibition of neural activity. Our dual-port detector is cost effective and easily replicable, and it should enable a wide variety of applications probing the neural circuit basis of sensory perception, motor action, and learning in normal and transgenic mouse models. NEW & NOTEWORTHY Mice readily learn tasks in which they respond to sensory cues by licking for liquid rewards; tasks that involve multiple licking responses allow study of neural circuits underlying decision making and sensory-motor integration. Here we design, characterize, and implement a novel dual-port lick detector that precisely measures directional licking in head-fixed mice performing visual behavior, enabling simultaneous neural recording and closed-loop manipulation of licking.

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