Divyan Bavan
Introduction
Sound provides critical information about an organism’s surroundings. While some sounds are monotonic, most sounds heard in nature are complex waveforms composed of many frequencies and amplitudes. Therefore, the ability to capture, process, and integrate auditory information is of utmost importance to many species. Humans are no exception. After capturing complex sound waves through the outer ear and middle ear, the inner ear processes and breaks them down. This information is then processed further through the superior olive, inferior colliculus, and medial geniculate nucleus. Finally, information reaches the primary auditory cortex (A1) in the temporal lobe. The intricacy of this pathway highlights specific features of complex sound waves that must be extracted, along with its overall importance in the body.
Processing in the Inner Ear
Sound waves reach the inner ear through the stapes: a bone in the middle ear which transmits sound vibrations to the cochlea. The cochlea is a coiled structure; its diameter decreases as it reaches the bony core (Kandel et al., 2021). The cochlea is composed of three compartments: the scala vestibuli, scala media, and scala tympani. In between the scala media and scala tympani is the basilar membrane. The Organ of Corti sits on top of this membrane; both are critical for processing sound. The scala media, which contains the endolymph fluid, is rich in potassium ions. This creates its high endocochlear potential of 80mV (JD’s Lecture Slides).
As mentioned previously, the basilar membrane sits in between the scala media and scala tymapani. As it travels along the cochlea towards the apex, it becomes wider and thinner. This leads to the basilar membrane being stiffer near the base. When sound waves travel along the membrane, they reach a high amplitude and then diminish; higher frequencies will reach this point sooner than low frequencies due to the stiffness gradient. Therefore, sound waves composed of multiple frequencies will produce multiple peaks along the basilar membrane. This is the first step to decomposing complex waveforms (Kandel et al., 2021).
To transmit these vibrations into electrical signals, the cochlea contains the Organ of Corti. It travels along the cochlea above the basilar membrane and below the tectorial membrane. To couple vibrations to electrical signals, it contains one row of inner hair cells (IHCs) and three rows of outer hair cells (OHCs). When the basilar membrane vibrates, it moves the Organ of Corti up and down. This causes shearing with the tectorial membrane. As the membrane slides over the hair cells, it causes the displacement of stereocilia. This opens stretch-sensitive potassium channels in the stereocilia. Since the electrochemical gradient for potassium between the endolymph and hair cells is very large, there is a large potassium influx into the cell. This leads to the opening of calcium channels and the release of glutamate at hair cell synapses (Kandel et al., 2021).
Hair cells (95% IHCs) synapse with spiral ganglion cells (SGCs): the first producers of action potentials in auditory processing. It is here that frequency and amplitude are encoded into electrical signals. This process uses three types of coding: rate, place, and temporal coding. Since IHCs use graded potentials, the amplitude of a sound can be encoded through how depolarized the cell is. This is then transferred to SGCs as a rate code; more depolarization leads to more frequent action potentials. While this accounts for amplitude, a separate mechanism must be used to encode frequency. This is done through a place code. As mentioned previously, the basilar membrane dissects complex sound waves through separating frequencies. Since separate hair cells and SGCs are placed along the membrane, this tonotopic organization is preserved as a place code. This works when the basilar membrane provides sharp frequency tuning, but this is not always the case. Low frequencies often spread across the membrane, making it hard to determine the correct pitch from place coding alone. To solve this, the auditory system uses temporal coding. When SGCs fire their action potentials, they prefer to do so at specific points of the waveform. This is called phase-locking, and is used to encode frequencies below 3kHz (Kandel et al., 2021).
Transmission to the Brain
Once SGCs collect information from the hair cells and transform them into neural codes, axons converge into the auditory nerve. This nerve then travels to the cochlear nucleus, where it contacts a variety of cells. These include bushy cells, multipolar cells, and onset cells; they preserve temporal codes, process frequency contrast, and encode sound amplitude, respectively (JD’s Lecture Slides).
Information from the cochlear nucleus then travels to the superior olive. This is the first centre for extracting information about differences between sounds from each ear. For example, the medial superior olive (MSO) is responsible for detecting interaural time differences. This area receives excitatory input from both the ipsilateral and contralateral auditory nerves and requires both inputs to maximally fire. However, due to differences in when signals arrive from each nerve, neurons in the MSO become tuned to distinct time differences. This can be used to encode information about where a sound is coming from, as sounds closer to one ear will arrive first. They will also be louder. These differences in amplitude are computed by the lateral superior olive (LSO). Unlike the MSO, the LSO receives inhibitory input from the contralateral side. This means that when a sound is closer to the ipsilateral side, neurons in the LSO will have a higher firing rate than if the sound intensity is greater on the contralateral side (JD’s Lecture Slides).
Neurons from the superior olive then transmit information to the inferior colliculus. This processing centre is important for auditory processing. However, its specific functions are still unknown (JD’s Lecture Slides). While we do know that specific non-auditory signals, such as engagement of motor systems, can influence the firing activity of neurons in the inferior colliculus, there is no unifying theory of its function. After processing occurs here, signals are transmitted to the medial geniculate body (MGB) of the thalamus. In this area of the thalamus, information from other sensory processes is integrated into auditory information. This creates a broader picture of the auditory scene (JD’s Lecture Slides).
The Auditory Cortex
Neurons from the MGB of the thalamus provide input to the primary auditory cortex (A1). At this point in the auditory pathway, coding is heavily modified. Although it is still tonotopically organized, A1 relies heavily on rate coding instead of temporal coding. This is because integration in the soma and dendrites of preceding neurons disrupts phase-locking; by the time signals reach A1, the maximum frequency able to be interpreted using phase-locking is less than 100Hz (Kandel et al., 2021). To compensate for this, A1 utilizes non-synchronized rate coding. Lu, Liang, and Wang showed that an awake marmoset has neurons that respond to low frequency clicks and separate neurons that respond to high frequency clicks. The latter fires at more frequent rates with increasing frequency of clicks. This enables better coding of temporal information (Kandel et al., 2021). This is important as the auditory cortex supports higher-order processes through sensory integration.
Conclusion
It is evident that the processing of auditory information is a highly complex process. Encoding starts in the cochlea, where complex sound waves are split into their fundamental frequencies. This enables place coding; spiral ganglion cells along the cochlea each collect information from a different frequency of sound. More detail is added through rate coding: the process of encoding sound amplitude into firing rate. Finally, information about low frequency sounds is distilled through temporal coding. This process aligns firing patterns to a phase of the sound wave. Once all this information has been encoded by the inner ear, it is sent to the brain for further processing. This pathway consists of the superior olive, inferior colliculus, MGB, and auditory cortex. These constituents process interaural time differences, interaural level differences, intersensory information, and more. Through understanding the complexities of these pathways, it is possible to build an appreciation for how important audition is to humans.
Works Cited
Kandel, Eric R. Principles of Neural Science. 6th ed., S.L., Mcgraw-Hill Education, 2021.
Dr. Johannes Dahmen’s Lecture Slides (Audition 1 and 2)