Spencer B. Smith
Au.D./Ph.D. student at the University of Arizona
*Please note: This article is Part I of a two-part series. Part II will be published as next month’s featured piece, so please be on the look-out!
Introduction:
Much of what is understood about the neurophysiology of auditory processing has been derived from studying and modeling the afferent auditory nervous system, a complex neural network that conveys information from the inner ears to the brainstem and cortex. However, a less extensive body of research in both experimental animals and humans suggests that the efferent auditory nervous system, a network descending from auditory cortex to the cochlea, may serve an equally important role in auditory processing.
One specific efferent circuit believed to be involved in the early stages of auditory processing is the olivocochlear system in the caudal brainstem. The olivocochlear system has two distinct subdivisions (see figure 1 in Guinan, 2006). Neurons from the medial olivocochlear (MOC) system project bilaterally from the periolivary nuclei of the medial superior olivary complexes to outer hair cells (OHCs). Activation of the MOC system decreases cochlear amplifier gain and thus indirectly reduces auditory nerve fiber discharge rates by altering basilar membrane motion patterns. Neurons from the lateral olivocochlear (LOC) system project from the periolivary nuclei of the lateral superior olivary complexes and synapse onto type I auditory nerve fibers. Activation of LOC neurons is believed to directly modulate auditory nerve fiber discharge rates by pharmacological means (Sahley et al., 1991).
Given that the caudal efferent system directly modulates cochlear mechanics and auditory nerve physiology, there has been much interest in developing clinical procedures to assay this system in humans. Such metrics may helpful in predicting a patient’s functional auditory abilities such as speech in noise perception (Giraud et al., 1997; Kumar & Vanaja, 2004), his or her resilience to noise-induced hearing loss (Lapsley-Miller et al., 2006), the onset of presbycusis (Zhu et al., 2007), or the expected benefit of auditory training exercises (de Boer & Thornton, 2008), to name a few examples. Many clinicians are curious if reliable assays of caudal efferent system function will ever be introduced to the clinic. What follows is an attempt to answer that question, presented in a two-part series. Part I will provide a brief overview of the anatomy and physiology of the caudal efferent system and review of some animal literature on the topic. Part II will provide a brief review of the human caudal efferent auditory system literature and end with a discussion regarding the progress and limitations of clinical assays of the caudal efferent system.
Historical Overview:
Animal Experiments –
Germinal experiments on the caudal efferent auditory system were performed using animal models. Rasmussen (1946) was the first to anatomically describe the olivocochlear efferents and Galambos (1956) first demonstrated that electrical stimulation of olivocochlear fibers resulted in a reduction of auditory nerve compound action potentials. Although replicated many times (Desmedt and Monaco, 1961; Fex, 1967; Desmedt, 1962; Wiederhold, 1970), this was a paradoxical finding, as the evolutionary benefit of such a reflex was not immediately clear. In the decades that followed, a more sophisticated understanding of the anatomy, pharmacology, and function of the efferent system was developed in animal models. Several putative roles of the mammalian caudal efferent system have been gleaned from this work.
Auditory Nerve “Unmasking”:
In the presence of masking noise, the dynamic range of auditory nerve fibers is reduced, as signal thresholds increase and saturation levels decrease due to synaptic depletion. Electrically or acoustically activating the caudal efferents, specifically the MOC system, desensitizes the auditory nerve to masking noise by reducing the cochlear excitation response to continuous broadband sounds. Thus, the “unmasking” effect of the MOC reflex restores the dynamic range of auditory nerve fibers and aids in the detection of transient signals in noise such as tones and speech (Kawase et al., 1993; Kawase and Liberman, 1993).
Resilience to Noise-Induced and “Hidden” Hearing Loss:
Animals raised in persistent, low-level acoustic stimulation were less likely to suffer cochlear damage when exposed to high levels of noise than animals living in quiet environments (Cody & Johnstone, 1982; Rajan & Johnstone, 1988). Presumably this is due to the “strengthening” of the caudal efferent system with low-level noise exposure (Brown et al., 1998), and there appears to be a positive relationship between MOC reflex strength and resilience to noise induced hearing loss (Maison & Liberman, 2000). This protective effect was abolished when the MOC system was either pharmacologically disabled or severed (Kujawa & Liberman, 1997). More recently, it was demonstrated that “hidden hearing loss” (i.e., suprathreshold hearing impairment due to auditory nerve fiber synaptopathy) was exacerbated in both noise exposed (Maison et al., 2013) and aging ears (Liberman et al., 2014) when the caudal efferent system was damaged. While this body of literature supports the role of the MOC system in protecting the ear from acoustic trauma, the LOC system may also reduce noise-induced excitotoxicity at the level of the inner hair cell/auditory nerve fiber synapse (Darrow et al., 2007; Ruel et al., 2001). Far less is known about the behavior and function of the LOC system due to the fact that the fibers are unmyelinated and in the minority among all olivocochlear neurons. Exciting work is underway examining the extent to which the caudal efferent system can be pharmacologically modulated, with the hope that prophylactic treatments against noise induced hearing impairments may be developed.
Top-down Control of Cochlear Processes During Attention:
As mentioned above, the efferent auditory system is extensive, beginning in the cortex and terminating at the level of the cochlea. This organization suggests that top-down influences, such as attention, may modulate cochlear function by “commandeering” the caudal efferent system. (Note that this organization, wherein a reflex is modulated by higher order brain centers, is ubiquitous in sensory systems. For example, the pupillary reflex is passively activated when photons are absorbed by the retina but can also be modulated during attention. Similarly, spinal reflexes can be “overridden” with attention). Delano and colleagues (2007) measured compound action potentials and cochlear microphonics from chinchillas during auditory and visual attention tasks. They found that compound action potential amplitude was significantly reduced while the cochlear microphonic was significantly increased during visual attention tasks compared with auditory attention tasks. Their explanation for these findings was that the MOC system increases the conductance of outer hair cells, and therefore simultaneously increases cochlear microphonic and decreases compound action potential amplitudes. Some, but not all, experiments have shown a decrease in auditory detection or discrimination after the olivocochlear system had been severed (May & McQuone, 1995).
Perhaps some of the most compelling data on the top-down effects of the efferent auditory system come from experiments in which neurons in the inferior colliculus were electrically stimulated. In some of these studies, otoacoustic emissions and auditory nerve compound action potentials were suppressed with activation of the efferent system “upstream” in the rostral brainstem (Mulders & Robertson, 2000; Rajan, 1990; Ota et al., 2004; Zhang & Dolan, 2006). Additionally, the best frequency of stimulated neurons in the inferior colliculus corresponded to the suppression frequency of otoacoustic and compound action potential measurements. Groff and Liberman (2003) reported long lasting neural suppression and enhancement with inferior colliculus stimulation, even in instances where otoacoustic emissions were unaltered. Furthermore, these findings persisted after selectively sectioning the MOC system, leading them to conclude that the LOC system may be involved in slow potentiation of auditory nerve responses. In summary, these studies provide evidence that attention and/or top-down modulation can alter hair cell and nerve fiber function and that this effect is mediated by a highly tuned descending network of efferent neurons.
Conclusion:
The mammalian caudal efferent system modulates afferent inputs at the earliest stages of auditory processing and can work both reflexively and under top-down control. While there are no doubt afferent-efferent interactions at every stage of the auditory nervous system, assays of the mammalian caudal efferent system have demonstrated that the olivocochlear bundle has potent effects on auditory processing and may bolster abilities such as listening in noise and selective attention. In Part II of this series, a brief review of human caudal efferent system experiments will be presented and the progress and limitations in developing a clinical test of human efferent function will be discussed.
Spencer B. Smith is an Au.D./Ph.D. candidate at the University of Arizona. His research examines the role of the human caudal efferent auditory system in the neural encoding of simple and complex stimuli in noisy environments. To support his research, Spencer has been awarded grants and scholarships from the National Institutes of Health (F30), the American Academy of Audiology Foundation, the American Speech-Language-Hearing Foundation, and the University of Arizona.
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