Auditory pathways

anatomy and physiology

James O. Pickles*    Department of Physiology and Pharmacology, School of Biomedical Sciences, University of Queensland, St. Lucia, Queensland, Australia
* Correspondence to: James O. Pickles, Department of Physiology and Pharmacology, School of Biomedical Sciences, University of Queensland, St. Lucia, Queensland 4072, Qld, Australia. email address: j.pickles@uq.edu.au

Abstract

This chapter outlines the anatomy and physiology of the auditory pathways. After a brief analysis of the external, middle ears, and cochlea, the responses of auditory nerve fibers are described. The central nervous system is analyzed in more detail. A scheme is provided to help understand the complex and multiple auditory pathways running through the brainstem. The multiple pathways are based on the need to preserve accurate timing while extracting complex spectral patterns in the auditory input. The auditory nerve fibers branch to give two pathways, a ventral sound-localizing stream, and a dorsal mainly pattern recognition stream, which innervate the different divisions of the cochlear nucleus. The outputs of the two streams, with their two types of analysis, are progressively combined in the inferior colliculus and onwards, to produce the representation of what can be called the "auditory objects" in the external world. The progressive extraction of critical features in the auditory stimulus in the different levels of the central auditory system, from cochlear nucleus to auditory cortex, is described. In addition, the auditory centrifugal system, running from cortex in multiple stages to the organ of Corti of the cochlea, is described.

Keywords

Hearing

anatomy

physiology

cochlea

cochlear nucleus

superior olive

inferior colliculus

medial geniculate

auditory cortex

review

Introduction and overview

The auditory brainstem, midbrain, and cortex have a multiplicity of parallel and overlapping pathways, which have parallel but overlapping and interrelated functions. In addition, the stages of analysis of the auditory signal are not as clearly separated or as clearly comprehensible as in for instance the visual system. It is difficult therefore to use a simple functional framework to help understand the anatomic and physiologic results. It is hoped that this chapter will provide a scheme by which the auditory system can be more easily approached and understood.

The auditory signal is a time-dependent variation in sound pressure. From the one-dimensional stimuli as received by each ear, the whole multifeatured auditory world is constructed. Therefore the auditory system accomplishes an outstanding feat of both analysis and synthesis. This chapter will describe some of the anatomy and physiology that underlies this. The issues described in this chapter are also described in more detail in An Introduction to the Physiology of Hearing, to which the reader is referred for further information (Pickles, 2012).

The outer and middle ears

The input impedance of the cochlea (defined as the pressure required to produce a unit displacement of the oval window) is some 200 times greater than that of free air (Nakajima et al., 2009). If the sound vibrations met the oval window directly, we can calculate that most of the energy would be reflected, with only 2% of the energy being transmitted. However, the outer and middle ears increase this transmission substantially. The increase in transmission is accomplished at two stages.

Firstly, the outer ear acts as a directionally sensitive ear trumpet, collecting sound pressures over the area of the pinna, and by a set of resonances, increasing the sound pressure at the rather smaller tympanic membrane. The frequency peaks of the major resonances are complementary, so that the pressure at the eardrum is raised relatively uniformly, by 15-20 dB, over the frequency range from 2 to 8 kHz, with transmission being similarly raised.

Secondly, there is an impedance transformer in the middle ear; this stage makes the major contribution. The middle-ear transformer has two components. Firstly, the largest factor arises from the ratio of the area of the tympanic membrane to the area of the footplate of the stapes in the oval window. The two areas are 60 mm2 and 3.2 mm2 respectively. The pressure on the oval window, and hence the pressure/displacement ratio, is therefore increased 60/3.2 = 18.75 times. The second factor is the lever action: the arm of the malleus (i.e., the umbo) is 2.1 times longer than the arm of the stapes. Therefore the force at the round window, and hence the pressure, is increased 2.1 times, while the displacement is decreased 2.1 times. The impedance ratio, being pressure/displacement, is therefore increased 2.12 = 4.4 times. The overall impedance change of the driving stimulus is therefore increased by 18.75 × 4.4 times = 82.5 times. The overall effect of the outer and middle ears is to increase the transmission efficiency, at its optimum frequency of 1 kHz, to 35% (Rosowski, 1991). Most of the losses in transmission are due to friction in the middle ear.

The absolute threshold and relation to outer- and middle-ear transmission

Over a wide range of frequencies, and in a variety of mammals, including human beings, the auditory absolute threshold corresponds to a power of the order of 10-18 W absorbed by the inner ear (Rosowski, 1991). Since at threshold we integrate energy for approximately 300 ms to make a decision, this equals an energy detection threshold of 3 × 10-19 J. This corresponds to the energy in a single quantum of red light. Therefore the fundamental energy sensitivities of the eye and the ear are comparable.

In young human beings with good hearing, the threshold of 10-18 W delivered to the cochlea applies over the range of 450 Hz to at least 10 kHz. Therefore, within this range the shape of the audiogram, i.e., the variation in the threshold of hearing as a function of frequency, can be described by the variation in the efficiency of transmission through the outer and middle ears to the inner ear. At higher and lower frequencies, however, other factors come into play. The upper frequency limit of hearing in human beings is commonly taken as 20 kHz in young children and 15 kHz in young adults (e.g., Dadson and King, 1952). The upper frequency limit of hearing arises because the cochlea itself becomes unresponsive to stimuli of higher frequency (Ruggero and Temchin, 2002). At low frequencies (< 1 kHz), the threshold rises gradually as the stimulus frequency is lowered, so there is no clear lower frequency limit of hearing. The gradually increasing threshold arises because below 1 kHz there is reduced transmission of power through the middle ear, and at still lower frequencies (< 450 Hz), the traveling wave reaches the apex of the cochlea. In this case, some of the power is shunted through the helicotrema, an opening between the scala vestibuli and the scala tympani at the extreme apex of the cochlea, and is not able to activate the hair cells.

The cochlea

Overall anatomy

The cochlea is a spiral fluid-filled tube, with (in human beings) 2.5 turns, an overall width of 1 cm, and standing 5 mm high. It is unfortunate that, following the well-known illustrations of Netter (1948), many common illustrations show the cochlea at about three times this size. The fluid-filled tube has three divisions or scalae, which spiral together around the central core, the modiolus, containing the auditory nerve and many of the blood vessels. One membrane between the scalae, the basilar membrane, contains the organ of Corti, the site of the receptor cells (Fig. 1.1). The spiral allows a long (35 mm long) basilar membrane and organ of Corti to be packed into a small overall dimension.

Anatomy in relation to function

The cochlea performs an amazing feat of sound detection and analysis. The absolute threshold mentioned above is many times lower than the thermal noise expected in the detector. Moreover, the cochlea performs a frequency analysis with a high degree of resolution, but without the long temporal "ringing" that would normally accompany such a high degree of frequency resolution.

The input vibrations of the cochlea produce the well-known traveling wave on the basilar membrane, which peaks more basally for stimuli of higher frequencies, and more apically for stimuli of lower frequencies (Fig. 1.2A). Therefore stimulus frequency is mapped on to place of stimulation in the cochlea. As originally measured by Békésy in human cadavers (see Békésy, 1960), the traveling wave was relatively small and...