Auditory fear conditioning alters neural gain in the cochlear nucleus: a wireless neural recording study in freely behaving rats.

Antonio G Paolini,Jee Hyun Kim,Simeon J Morgan

doi:10.1042/ns20200009

Abstract

Anxiety disorders involve distorted perception of the world including increased saliency of stress-associated cues. However, plasticity in the initial sensory regions of the brain following a fearful experience has never been examined. The cochlear nucleus (CN) is the first station in the central auditory system, with heterogeneous collections of neurons that not only project to but also receive projections from cortico-limbic regions, suggesting a potential for experience-dependent plasticity. Using wireless neural recordings in freely behaving rats, we demonstrate for the first time that neural gain in the CN is significantly altered by fear conditioning to auditory sequences. Specifically, the ventral subnuclei significantly increased firing rate to the conditioned tone sequence, while the dorsal subnuclei significantly decreased firing rate during the conditioning session overall. These findings suggest subregion-specific changes in the balance of inhibition and excitation in the CN as a result of conditioning experience. Heart rate was measured as the conditioned response (CR), which showed that while pre-conditioned stimulus (CS) responding did not change across baseline and conditioning sessions, significant changes in heart rate were observed to the tone sequence followed by shock. Heart-rate findings support acquisition of conditioned fear. Taken together, the present study presents first evidence for potential experience-dependent changes in auditory perception that involve novel plasticity within the first site of processing auditory information in the brain.

Highlights

The ability to modulate attention to biologically significant stimuli is critical for survival
Interaction was investigated with post hoc tests controlling for family-wise error rate (FWER; due to the huge number of bins = 161), which showed that conditioned stimulus (CS)+ tones initially resulted in significantly decreased heart rate at 2.7–2.9 s from CS onset and increased heart rate compared CS− tones during 6.5–8.0 s from mismatch onset (Figure 4A, *Ps
We have discovered the presence of neurons in cochlear nucleus (CN) that show plasticity to alternating frequencies of tone paired with shock

Summary

Introduction

The ability to modulate attention to biologically significant stimuli is critical for survival Such a stimulus may be intrinsically salient, or may be initially neutral but become salient due to its association with important events. Fear conditioning has been extensively utilized in humans and rodents to study the potential role of emotional associative memory in anxiety disorders and post-traumatic stress disorder [1–7]. While it has been proposed as a useful tool to understand hypervigilance toward cues associated with stressful and/or anxious experience [3,4], how conditioned fear experience may contribute to vigilance at the neural level is poorly understood. In the case of tone-fear conditioning, the LA receives auditory information via two well-characterized parallel pathways both of which involve the medial geniculate nucleus of the thalamus (MGN). One pathway consists of the auditory cortex areas that receive input from the MGN and that project to the LA, forming the thalamic-cortico-amygdala

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Conclusion