Abstract
The acoustic startle reflex (ASR) is a survival mechanism of alarm, which rapidly alerts the organism to a sudden loud auditory stimulus. In rats, the primary ASR circuit encompasses three serially connected structures: cochlear root neurons (CRNs), neurons in the caudal pontine reticular nucleus (PnC), and motoneurons in the medulla and spinal cord. It is well-established that both CRNs and PnC neurons receive short-latency auditory inputs to mediate the ASR. Here, we investigated the anatomical origin and functional role of these inputs using a multidisciplinary approach that combines morphological, electrophysiological and behavioral techniques. Anterograde tracer injections into the cochlea suggest that CRNs somata and dendrites receive inputs depending, respectively, on their basal or apical cochlear origin. Confocal colocalization experiments demonstrated that these cochlear inputs are immunopositive for the vesicular glutamate transporter 1 (VGLUT1). Using extracellular recordings in vivo followed by subsequent tracer injections, we investigated the response of PnC neurons after contra-, ipsi-, and bilateral acoustic stimulation and identified the source of their auditory afferents. Our results showed that the binaural firing rate of PnC neurons was higher than the monaural, exhibiting higher spike discharges with contralateral than ipsilateral acoustic stimulations. Our histological analysis confirmed the CRNs as the principal source of short-latency acoustic inputs, and indicated that other areas of the cochlear nucleus complex are not likely to innervate PnC. Behaviorally, we observed a strong reduction of ASR amplitude in monaural earplugged rats that corresponds with the binaural summation process shown in our electrophysiological findings. Our study contributes to understand better the role of neuronal mechanisms in auditory alerting behaviors and provides strong evidence that the CRNs-PnC pathway mediates fast neurotransmission and binaural summation of the ASR.
Highlights
The acoustic startle reflex (ASR) is a survival mechanism of alarm, which rapidly alerts and arouses organisms to a sudden loud auditory stimulus
We examined the course of HRP-labeled axons within the cochlear root nucleus, and found that they give off collaterals of various diameters and numerous endings that terminated on cochlear root neurons (CRNs) somata, but not exclusively (Figures 2A1,A2)
The cochlear nerve collaterals were orientated perpendicular to the parent fibers, and extended approximately 70 μm in length to innervate the cell body of CRNs immunostained for calbindin protein-D28K (CaBP) (Figures 2A3,A4)
Summary
The acoustic startle reflex (ASR) is a survival mechanism of alarm, which rapidly alerts and arouses organisms to a sudden loud auditory stimulus. The cochlear root neurons (CRNs), true sentinels of the rodent auditory pathway, are the first brainstem neurons receiving direct input from spiral ganglion cells (Harrison et al, 1962; Merchán et al, 1988; Osen et al, 1991; López et al, 1993, 1999). They comprise the so-called cochlear root nucleus, and are morphologically characterized by their large cell body and thick dendrites that distribute among the eighth nerve fibers (Merchán et al, 1988; López et al, 1993). The acoustically driven PnC neurons project to facial, cranial and spinal motoneurons that rapidly activate the muscle contractions
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