Corticofugal modulation of peripheral auditory responses

Abstract

The auditory efferent system originates in the auditory cortex and projects to the medial geniculate body (MGB), inferior colliculus (IC), cochlear nucleus (CN) and superior olivary complex (SOC) reaching the cochlea through olivocochlear (OC) fibers. This unique neuronal network is organized in several afferent-efferent feedback loops including: the (i) colliculo-thalamic-cortico-collicular; (ii) cortico-(collicular)-OC; and (iii) cortico-(collicular)-CN pathways. Recent experiments demonstrate that blocking ongoing auditory-cortex activity with pharmacological and physical methods modulates the amplitude of cochlear potentials. In addition, auditory-cortex microstimulation independently modulates cochlear sensitivity and the strength of the OC reflex. In this mini-review, anatomical and physiological evidence supporting the presence of a functional efferent network from the auditory cortex to the cochlear receptor is presented. Special emphasis is given to the corticofugal effects on initial auditory processing, that is, on CN, auditory nerve and cochlear responses. A working model of three parallel pathways from the auditory cortex to the cochlea and auditory nerve is proposed.

Keywords: auditory efferent; corticofugal; descending projections; neural network; olivocochlear; top-down.

Figure 1

Schematic diagram of the auditory efferent network. Ascending and descending pathways are depicted in black and red arrows respectively. A simplified model of the auditory efferent system is presented. Corticofugal projections from the auditory cortex to the inferior colliculus (IC) and medial geniculate body (MGB) and afferent connections from the IC and MGB to the auditory cortex form a “top loop” within this network (colliculo-thalamic-cortico-collicular loop, Xiong et al., 2009). Bottom loops are constituted by auditory-cortex descending projections to the CN (cortico-(collicular)-cochlear nucleus loop) and SOC (cortico-(collicular)-olivocochlear loop), which are connected to the cochlear receptor by the OC bundle. Note, the relevant position of the IC in the interaction between top and bottom loops. In addition, it is important to highlight that cortical modulations of cochlear responses, can modify IC responses through ascending connections to the CN and IC, meaning that the interaction between the top and bottom loops is bidirectional. CN: cochlear nucleus; IC: inferior colliculus; MGB: medial geniculate body; SOC: superior olivary complex.

Figure 2

The three pathways model for the cortico-collicular-olivocochlear and cochlear nucleus circuits. In order to simplify this model, the colliculo-thalamic-cortico-collicular loop has been omitted. In addition, only efferent pathways from the left auditory cortex to the right cochlea are presented. Three OC pathways are directed to the right cochlear receptor and auditory nerve, which are depicted in color green, orange and blue corresponding to the: (i) right LOC fibers; (ii) right uncrossed MOC; and (iii) left crossed MOC neurons respectively. Ipsilateral acoustic stimulation of the right cochlea activates right AN, right CN neurons that send projections to the contralateral MOC. In turn, left crossed MOC neurons modulate right cochlear responses (blue brainstem pathways), constituting the ipsilateral OC reflex. On the other hand, contralateral acoustic stimulation of the left cochlea activates, left AN, left CN neurons that send projections to the right uncrossed MOC fibers, which modulate right cochlear responses (orange brainstem pathways), constituting the contralateral OC reflex that connects both ears. This model proposes that the descending pathways from the left auditory cortex directed to the left IC and to the left CN (orange corticofugal pathways) modulate the contralateral OC reflex, by regulating the activity of the left CN and right uncrossed MOC neurons. On the other hand, descending pathways directed to the left IC and left MOC (blue corticofugal pathways) regulate crossed MOC activity, which is involved in the ipsilateral OC reflex. Finally, corticofugal pathways to the contralateral IC (green corticofugal pathways) could regulate right LOC neurons, modulating the activity of right AN fibers. The +/− signs represent possible excitatory and inhibitory pathways. Modified from Dragicevic et al. (2015) with permission. AN: auditory nerve; CN: cochlear nucleus; LOC: lateral olivocochlear; MOC: medial olivocochlear; IC: inferior colliculus.