Abstract
Sensorimotor integration is a pivotal feature of the nervous system for ensuring a coordinated motor response to external stimuli. In essence, such neural circuits can optimize behavioral performance based on the saliency of environmental cues. In zebrafish, habituation of the acoustic startle response (ASR) is a simple behavior integrated into the startle command neurons, called the Mauthner cells. Whereas the essential neuronal components that regulate the startle response have been identified, the principles of how this regulation is integrated at the subcellular regions of the Mauthner cell, which in turn modulate the performance of the behavior, is still not well understood. Here, we reveal mechanistically distinct dynamics of excitatory inputs converging onto the lateral dendrite (LD) and axon initial segment (AIS) of the Mauthner cell by in vivo imaging glutamate release using iGluSnFR, an ultrafast glutamate sensing fluorescent reporter. We find that modulation of glutamate release is dependent on NMDA receptor activity exclusively at the AIS, which is responsible for setting the sensitivity of the startle reflex and inducing a depression of synaptic activity during habituation. In contrast, glutamate-release at the LD is not regulated by NMDA receptors and serves as a baseline component of Mauthner cell activation. Finally, using in vivo calcium imaging at the feed-forward interneuron population component of the startle circuit, we reveal that these cells indeed play pivotal roles in both setting the startle threshold and habituation by modulating the AIS of the Mauthner cell. These results indicate that a command neuron may have several functionally distinct regions to regulate complex aspects of behavior.
Highlights
Special neural circuits enable the animal to effectively distinguish sensory information based on saliency before making a behavioral decision
Habituation of the acoustic startle response in zebrafish has been previously suggested to be regulated by depression of synaptic activity at the lateral dendrite (LD) (Marsden and Granato, 2015), the exact role of converging excitatory processes of the circuit was not fully understood
We found that the two subcellular compartments exert strikingly distinct characteristics in setting the startle threshold and habituation (Figure 6)
Summary
Special neural circuits enable the animal to effectively distinguish sensory information based on saliency before making a behavioral decision. One pivotal example of sensorimotor integration is habituation, a simple form of non-associative learning, manifested as the progressive decline of a particular behavioral response to repeated sensory stimulation (Thompson and Spencer, 1966; Giles and Rankin, 2009). Many studies have provided insights into the possible cellular mechanisms behind the progressive attenuation of behavioral responses during habituation (Krasne and Bryan, 1973; Stopfer et al, 1996; Weber et al, 2002; Ezzeddine and Glanzman, 2003; Bristol and Carew, 2005). The model of homosynaptic depression, for example, suggests that it is the depletion of the pool of presynaptic neurotransmitter vesicles that leads to the attenuation of a monosynaptic circuit and drives habituation. The gradual potentiation of a feedforward inhibitory neuron population is presented as the source of the modulation of the excitability of the neuron controlling the behavioral output
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