Abstract

Understanding how the brain controls behavior requires observing and manipulating neural activity in awake behaving animals. Neuronal firing is timed at millisecond precision. Therefore, to decipher temporal coding, it is necessary to monitor and control animal behavior at the same level of temporal accuracy. However, it is technically challenging to deliver sensory stimuli and reinforcers as well as to read the behavioral responses they elicit with millisecond precision. Presently available commercial systems often excel in specific aspects of behavior control, but they do not provide a customizable environment allowing flexible experimental design while maintaining high standards for temporal control necessary for interpreting neuronal activity. Moreover, delay measurements of stimulus and reinforcement delivery are largely unavailable. We combined microcontroller-based behavior control with a sound delivery system for playing complex acoustic stimuli, fast solenoid valves for precisely timed reinforcement delivery and a custom-built sound attenuated chamber using high-end industrial insulation materials. Together this setup provides a physical environment to train head-fixed animals, enables calibrated sound stimuli and precisely timed fluid and air puff presentation as reinforcers. We provide latency measurements for stimulus and reinforcement delivery and an algorithm to perform such measurements on other behavior control systems. Combined with electrophysiology and optogenetic manipulations, the millisecond timing accuracy will help interpret temporally precise neural signals and behavioral changes. Additionally, since software and hardware provided here can be readily customized to achieve a large variety of paradigms, these solutions enable an unusually flexible design of rodent behavioral experiments.

Highlights

  • Mechanistic insight about brain function often comes from accurate recordings of action potentials fired by neurons at millisecond order temporal precision

  • We provide here a complete modular head-fixed design for combined behavior, electrophysiology and optogenetic experiments in mice (Figure 3)

  • We opted for the photosensor/photodiode solution in order to avoid the introduction of electric artifacts to the electrophysiology recordings and because the same port structure could be employed for head-fixed and freely behaving paradigms

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Summary

Introduction

Mechanistic insight about brain function often comes from accurate recordings of action potentials fired by neurons at millisecond order temporal precision. One can only hope to extract specific information about external variables carried by spike timing (Arabzadeh et al, 2006; Panzeri et al, 2017) if behaviorally relevant events of the task, like cue stimuli (Ranade and Mainen, 2009; Jaramillo and Zador, 2011; Raposo et al, 2012; Brunton et al, 2013; Hanks et al, 2015), go and stop instructions (Lin and Nicolelis, 2008), reward and punishment delivery (Cohen et al, 2012; Raposo et al, 2012; Pi et al, 2013; Hangya et al, 2015) are under the same precision of temporal control. This intuition is formally captured by Shannon’s framework of information channel capacity, known as the ‘Shannon limit,’ which quantifies the maximal rate of error-free information transfer through a channel with given bandwidth and noise (Csiszár and Körner, 2011)

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