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The Olivocochlear Reflex Strength in Awake Chinchillas Is Relevant For www.nature.com/scientificreports OPEN The olivocochlear refex strength in awake chinchillas is relevant for behavioural performance during visual selective attention with auditory distractors Macarena Bowen1,3, Gonzalo Terreros4, Felipe N. Moreno‑Gómez5, Macarena Ipinza1, Sergio Vicencio1, Luis Robles7 & Paul H. Delano1,2,6,8* The auditory eferent system comprises descending projections from the cerebral cortex to subcortical nuclei, reaching the cochlear receptor through olivocochlear fbres. One of the functions attributed to this corticofugal system is to suppress irrelevant sounds during selective attention to visual stimuli. Medial olivocochlear neurons can also be activated by sounds through a brainstem refex circuit. Whether the individual variability of this refex is related to the cognitive capacity to suppress auditory stimuli is still controversial. Here we propose that the individual strength per animal of the olivocochlear refex is correlated with the ability to suppress auditory distractors during visual attention in awake chinchillas. The olivocochlear refex was elicited with a contralateral broad‑band noise at ~ 60 dB and ipsilateral distortion product otoacoustic emissions were obtained at diferent frequencies (1–8 kHz). Fourteen chinchillas were evaluated in a behavioural protocol of visual attention with broad‑band noise and chinchilla vocalizations as auditory distractors. Results show that the behavioural performance was afected by both distractors and that the magnitudes of the olivocochlear refex evaluated at multiple frequencies were relevant for behavioural performance during visual discrimination with auditory distractors. These results stress the ecological relevance of the olivocochlear system for suppressing natural distractors. Attention is a cognitive function that works as a biological flter allowing us to select relevant stimuli from the environment and to partially ignore the rest 1. Attention can be mediated by top-down and bottom-up neural mechanisms, depending on whether the cognitive process is driven by a voluntary goal or by the stimulus sali- ence, respectively2. It has been proposed that top-down processing during selective attention modulates sensory responses at diferent levels of the nervous system maintaining task-directed behaviour2,3. Cross-modal paradigms of visual selective attention with auditory distractors have demonstrated changes in neural activity at diferent levels of the auditory pathway, including cortical regions4–6, subcortical nuclei7, auditory nerve, and the cochlear receptor8,9. Previously, we demonstrated in chinchillas that selective attention to visual stimuli modulates the amplitude of auditory-nerve compound action potentials and cochlear micro- phonics, most likely through the activation of the auditory eferent system9. 1Departamento de Neurociencia, Facultad de Medicina, Universidad de Chile, Santiago, Chile. 2Departamento de Otorrinolaringología, Hospital Clínico de la Universidad de Chile, Santiago, Chile. 3Departamento de Fonoaudiología, Facultad de Medicina, Universidad de Chile, Santiago, Chile. 4Instituto de Ciencias de la Salud, Universidad de O’Higgins, Rancagua, Chile. 5Laboratorio de Bioacústica y Ecología del Comportamiento Animal, Departamento de Biología y Química, Facultad de Ciencias Básicas, Universidad Católica del Maule, Talca, Chile. 6Biomedical Neuroscience Institute, BNI. Facultad de Medicina, Universidad de Chile, Santiago, Chile. 7Programa de Fisiología y Biofísica, ICBM, Facultad de Medicina, Universidad de Chile, Santiago, Chile. 8Centro Avanzado de Ingeniería Eléctrica y Electrónica, AC3E, Universidad Técnica Federico Santa María, Valparaíso, Chile. *email: [email protected] SCIENTIFIC REPORTS | (2020) 10:14894 | https://doi.org/10.1038/s41598-020-71399-8 1 Vol.:(0123456789) www.nature.com/scientificreports/ Te auditory eferent system is a neural network that comprises descending projections from the auditory cortex to the inferior colliculus, cochlear nucleus and superior olivary complex 10–12, from where the medial olivocochlear (MOC) bundle emerges making synapses directly with outer hair cells of the cochlea 13. Te func- tionality of these corticofugal pathways has been demonstrated in bats, chinchillas and humans 14–17, and these descending projections are proposed to be the mediators of selective attention top-down efects on the cochlear receptor18,19. In addition, peripheral modulations of the cochlear receptor during visual attention have been demonstrated in humans20–22. For example, Wittekindt et al. (2014) showed that during periods of visual atten- tion the amplitude of distortion product otoacoustic emissions (DPOAE) was reduced whereas during auditory attention their amplitude remained unchanged. Medial olivocochlear fbres can be activated by ipsilateral and contralateral acoustic stimulation (CAS), producing a suppressive efect on cochlear responses, that is highly variable among diferent individuals 23. Previ- ously, we showed that larger suppressions of auditory nerve responses by contralateral broad-band noise (BBN) are associated with better performance in a visual selective attention task with auditory distractors in mice18. However, in that work, the MOC refex was evaluated in anesthetized mice, a condition that is known to under- estimate olivocochlear efects24,25. Additionally, whether the correlations between the individual strength of the olivocochlear refex and the cognitive capacity to avoid auditory distractors are frequency specifc or greater with ecologically relevant auditory distractors is unknown. Here, we measured the contralateral acoustic suppression of DPOAEs with broad-band noise in awake chin- chillas and evaluated their behavioural performance in a visual selective attention task using two diferent audi- tory distractors: broad-band noise and chinchilla distress vocalizations (VOC)26 (Fig. 1). Our results indicate that the efects of contralateral noise on multiple DPOAE frequencies in awake chinchillas are relevant for predicting behavioural performance in a visual selective attention task with both types of auditory distractors. Results Behavioural performance with auditory distractors. Figure 2 shows the efects of BBN and VOC in the behavioural performance of chinchillas (n = 14) during the 12 days of the experimental protocol, show- ing that there were signifcant efects in days 5 and 9. To facilitate the reading of the results, each day of the protocol will be referred using the acronym of the three stages (BL (for baseline), BBN and VOC) followed by the number 1 to 4, corresponding to the day of presentation (e.g.: day 1 = BL1, day 9 = VOC1). Te generalized linear mixed efects models (GLMM) showed an efect of the stage of behavioural protocol on the number 2 2 of correct responses (X (2) = 30.818, p < 0.0001) and omissions (X (2) = 38.528, p < 0.0001). For these two vari- ables, signifcant a posteriori Tukey pairwise tests were found for the comparisons between BL1 and BBN1, and between BL1 and VOC1, but not between BBN1 and VOC1 (Table 1). For accuracy, there was also an efect of the 2 stage of behavioural protocol (X (2) = 285.657, p < 0.0001), and all pairwise comparisons (BL1-BBN1, BL1-VOC1 and BBN1-VOC1) showed signifcant diferences (Table 1). Regarding latency, the linear mixed efects models 2 (LMM) analysis showed a signifcant efect of the stage of behavioural protocol (X (2) = 9.671, p = 0.008), where the only signifcant pairwise diference was obtained between BL1 and VOC1 latencies (Table 1). Consequently, the results shown in Fig. 2 and Table 1 evidence that both auditory distractors signifcantly disrupted the behav- ioural performance of chinchillas during the visual discrimination task. CAS efects on DPOAE. Te MOC refex strength is referred as the dB of change between the DPOAE amplitudes with and without CAS, a measure that was obtained before the behavioural protocol, with amplitude reductions as negative values. Animals were kept awake and unanaesthetised during all the DPOAE measure- ments, since evidence shows that the MOC refex strength is underestimated in anesthetized chinchillas 25. Fig- ure 3 shows the efects of contralateral acoustic stimulation on DPOAE amplitudes for frequencies between 1 and 8 kHz. An average CAS efect of − 1.28 ± 1.75 dB (mean ± SEM) was obtained across frequencies, with larger efects at 4 kHz (− 2.16 ± 0.57 dB) and 6 kHz (− 2.05 ± 0.60 dB). Medial olivocochlear refex strength and behavioural performance. Next, we studied whether the individual variability in the strength of contralateral acoustic suppression in awake chinchillas could be a predictor of behavioural performance in the visual task with auditory distractors. To evaluate the efect of each auditory distractor on the behavioural performance we chose the frst day of presentation of the distractor as the measure of interest (BBN1 and VOC1), based on the daily results observed during the 12 days of experimen- tal protocol (Fig. 2). Generalized linear models were used to assess whether the diferent DPOAE frequencies and the individual variability of the olivocochlear refex strength could account for the individual behavioural performance. Models obtained by stepwise backward selection for broad-band noise (BBN1) show that the mag- nitudes of the olivocochlear refex evaluated at multiple DPOAE frequencies are relevant for the number of correct responses, omissions and accuracy during the selective attention task (Table 2). In relation to the latency of correct responses, only
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