SPH307 Auditory Physiology and Psychoacoustics Dr Robert H. Mannell Department of Linguistics Macquarie University

The Brainstem Auditory Nuclei
and Centrifugal Pathways

Terminology

Click here for an explanation of some of the terminology used in this lecture.

Readings

The readings for this lecture are as follows:-

1. Brainstem Auditory Nuclei: Pickles (1988), chapter 6.
2. Centrifugal Pathways: Pickles (1988), chapter 8.

Themes in the Analysis of Sensory Systems

1. Feature detection - selective extraction (onsets, amplitude/frequency modulation)
2. Functional localisation in specific cells. That is, cells that respond to specific features. There are two extreme of viewpoints that illustrate this theme:-
   1. Each cell represents a point in feature space: This means that each cell is associated with a single acoustic or higher-level (more abstract) feature.
   2. Each cell represents many points in feature space: This model assumes that features are represented in a distributed network where each cell, with its many connections, is associated with more than one feature.
3. Hierarchical processing - successively more complex processing at higher levels

Types of Responses of Auditory Brainstem Nuclei

1. neural temporal firing patterns
2. neural frequency resolution
3. excitatory-inhibitory interactions
4. response to complex stimuli
5. binaural interactions

Ipsilateral and Contralateral Interactions in the Brainstem

Figure 1: An overview of afferent ipsilateral and contralateral interactions in the auditory brainstem.

Cochlear Nuclei

Each auditory fibre branches: one branch projects rostrally, one branch projects caudally.

Rostral branch:- antereoventral cochlear nucleus (AVCN)

Caudal branch:-

1. posteroventral cochlear nucleus (PVCN)
2. dorsal cochlear nucleus (DCN)

All three cochlear nuclei exhibit tonotopic mapping of frequency, but:-

• AVCN - simple tonotopicity - (simple relay of frequencies to higher centres)
• DCN - more complex response patterns - bypass superior olivary complex
• PVCN - pattern of tonotopicity is intermediate to that of AVCN and DCN

Cell types in Cochlear Nuclei

A number of cell types have been identified and characterised by their shape and size. These cell types include:-

1. large spherical cells
2. small spherical cells
3. globular cells
4. octopus cells
5. giant cells

Cells in the cochlear nuclei can be classified by their temporal response. Post-stimulus time histograms (PSTH) examine the response of a neuron to a stimulus (often a tone or a band of noise). In the cochlear nuclei, a number of classes of neuron, based on their temporal response, have been identified. They are:-

1. primary-like cells (ie. like the primary neurons of the auditory nerve) - post stimulus response similar to auditory nerve fibres (especially in the AVCN and PVCN)
2. onset responses - respond to sudden increase in amplitude (eg. onset of tone burst) eg. octopus cells - only onset responses
3. chopper responses - fire repetitively "at a rate unrelated to" stimulus period
4. pauser and builder responses - in fusiform layer of DCN - complex excitatory and inhibitory inputs

Inhibition

Inhibition of the primary-like cells of the AVCN shows similar patterns to the inhibition of the primary auditory nerve fibres. Inhibitory patterns show an excitatory response area and inhibitory sidebands.

Some frequency/intensity values excite certain types of neuron.

Other frequency/intensity values inhibit those neurons (sidebands).

Two Functional Aspects of the Cochlear Nuclei

1) ventral cochlear nucleus - simple tonotopic response - feeds to superior olivary complex where temporal analysis occurs

2) dorsal cochlear nucleus - complex frequency analysis bypasses superior olivary complex and goes directly to lateral lemniscus and inferior colliculus

Superior Olivary Complex

The Superior Olivary Complex consists of the Medial Nucleus of the Superior Olive (MSO), the Lateral Nucleus of the Superior Olive (LSO) and the Medial Nucleus of the Trapezoid Body (MTB). It also consists of a number of pre-olivary and peri-olivary nuclei which receive mostly efferent innervation.

Fibres from the DCN and some of the fibres from the PVCN bypass the Superior Olive Complex. Fibres from the AVCN (and some fibres from the PVCN) project to the ipsilateral LSO and MSO and to the contralateral MSO and (via the contralateral MTB) to the contralateral LSO. (see Pickles, 1998, figs 6.8 and 6.9, pp 180-181).

In the MSO and the LSO there are two major types of neuron:-

1. "EE" (Excited-Excited) cells are excited by signals from both ears.
2. "EI" (Excited-Inhibited) cells are excited by signals from the ipsilateral ear and inhibited by signals from the contralateral ear.

Medial Nucleus of Superior Olive (MSO)

The MSO mainly receives innervation from both the ipsilateral and the contralateral AVCN.

The MSO has a tonotopic response pattern that favours low frequencies. This particularly enhances the MSO's analysis of interaural temporal disparities in a waveform as low frequencies better preserve phase information.

The majority of MSO cells are EE cells, but there is also a significant minority of EI cells.

MSO EE cells determine the direction that a signal comes from on the basis of interaural timing (phase) differences.

EE cells display:-

• cyclic dependence (cyclic phases of inhibition and excitation)
• characteristic delay
• strongest response when synchronised signal from both ears

Different EE cells appear to have different "characteristic delay" and respond most strongly when the delay between the two ears matches this delay time. That is, when the phase difference between the two ears matches the characteristic delay time of the cell the signals from each ear appear to that cell to be aligned and thus the signals from the two ears reinforce each other to the greatest degree.

Lateral nucleus of Superior Olive (LSO)

The LSO mainly receives innervation from both the ipsilateral the contralateral AVCN. Innervation from the contralateral AVCN is via the ipsilateral MTB.

In the LSO, most cells are EI cells.

The LSO analyses interaural intensity differences. LSO EI neurons respond to these interaural intensity differences. When the interaural intensity difference is least (for signals on the medial plane) the signal from the contralateral ear most effectively cancels out signal from the ipsilateral ear.

The LSO cells are also sensitive to interaural timing differences although this appears to be a secondary function of the LSO.

The LSO has a tonotopic response pattern that favours high frequencies. This particularly enhances the LSO's analysis of interaural intensity disparities as intensity differences are greatest at high frequencies because higher frequencies experience less diffraction around the head.

Medial Nucleus of Trapezoid Body (MTB)

The MTB is a passive relay which conveys information from the cochlear nucleus of contralateral ear.

Lateral Lemniscus

The Lateral Lemniscus has two main nuclei:-

Ventral Nucleus - Input from the contralateral Cochlear Nucleus and output to the ipsilateral Inferior Colliculus.

Dorsal Nucleus - Bilateral input from the Cochlear Nucleus and bilateral output to the Inferior Colliculus.

Inferior Colliculus

The Inferior Colliculus (IC) is an auditory relay and auditory reflex centre.

Three divisions:-

1. Central Nucleus (CN) - specialised auditory pathway. The Central Nucleus combines the "complex frequency analysis of the dorsal cochlear nucleus with the sound localising ability of the superior olive.
   
   
2. Dorsal Cortex - auditory and somatosensory input - diffuse auditory pathway.
   
   
3. Paracentral Nuclei (including the Dorsomedial Nucleus DN) - diffuse auditory pathway - shared with somatic senses.

The Central nucleus is characterised by iso-frequency sheets (see Pickles, fig. 6.16c, p190). Each of these sheets represent a single characteristic frequency (cf), with low CF sheets rostrally and high CF sheets caudally. This suggests the possibility of multiple, parallel, representations of each frequency represented in a three dimensional matrix where one dimension (caudal to rostral) represent frequency whilst the other two dimensions represent some other parameters (eg. signal direction). It may be that this structure is a map of frequency in space.

The Dorsal Cortex and the Paracentral Nuclei are the most peripheral examples of a diffuse or non-specific auditory system surrounding the specific or core auditory system. The diffuse or nonspecific parts of the auditory system have auditory as well as other input. Little is known about the function of these diffuse auditory centres.

Pickles (1988) speculates on the function of the Inferior Colliculus (and specifically the Central Nucleus) as follows:-

"Localizing sound by interaural time disparities requires the preservation of accurate time relations. These are lost in the dorsal cochlear nuclear nucleus by the circuitry needed for complex amplitude and frequency analysis. It is therefore appropriate that the direction of the sound should be extracted separately. The inferior colliculus, by combining information from both sources, might therefore be able to code simultaneously the complexity of sounds and their direction in space." (p194)

Medial Geniculate Body

The Medial Geniculate Body accepts afferents from Inferior Colliculus and projects to cerebral cortex.

The Medial Geniculate Body can be divided into three regions:-

Ventral Division (v) - The Ventral Division is a specific auditory relay with input from the Inferior Colliculus and it projects principally to AI area of auditory cortex.

Dorsal Division (d) - Diffuse auditory division with both auditory (Inferior Colliculus) and non-auditory (eg. somatosensory) input. Has projections to the AII area of the auditory cortex.

Medial Division (m) - Diffuse auditory division with both auditory (pericentral nucleus of the Inferior Colliculus) and non-auditory (eg. somatosensory) input. The medial division has nonspecific projections to auditory cortex.

The Ventral Division is tonotopically organised.

Some neurons have complex temporal properties.

Some neurons are binaurally sensitive.

Some neurons are sensitive to interaural intensity differences (high frequency).

Some neurons are sensitive to interaural time differences (low frequency).

Auditory Reflexes

1. Unlearned Reflexes
   1. a) middle ear muscle reflex - stapedius muscle contracts reflexively to loud sounds. The Ventral Cochlear Nucleus projects to the MSO which, in response to a loud stimulus, generates an efferent signal to the motor nuclei of the facial and trigeminal nerves.
   2. b) auditory startle response
   3. c) directs attention to auditory shock
2. Learned Reflexes

Centrifugal Pathways

The auditory centrifugal pathways are efferent or descending pathways that carry information from more central to more peripheral levels of the auditory system.

The auditory centrifugal pathways run close to, but usually not within, the tracts containing the auditory afferent pathways.

Efferent pathways enable more central processes to influence more peripheral processes. Such affects might include:-

1. feedback loops that act in response to input signals
2. central influencing of peripheral sensation - eg. attention

The Olivocochlear Bundle

This centre is found in the Superior Olivary Complex of the brainstem and the efferent neurons that arise in this bundle have their point of origin around, but not within, the afferent nuclei (MSO, LSO, MTB) as well as in the pre-olivary and peri-olivary nuclei.

The cells of the olivocochlear bundle are differentiated into different types:-

1. small cells (around the LSO): project to the nerve fibres below the inner hair cells
2. large cells (around the MSO): project to the outer hair cells

Figure 2: An overview of the Efferent connections of the Olivocochlear Bundles from the left and right Olivary regions to the left and right cochlea. Two bundles of fibres descend from each side. The Crossed Olivocochlear Bundles (COCB) represent about 1/3 of the fibres and the Uncrossed Olivocochlear Bundles (UCOCB) represent about 2/3 of the fibres originating on each side. Other fibres not represented in this diagram make up the remaining 6%.

The olivocochlear bundles:-

1. reduce hair cell membrane resistance, opening K+ and Cl- channels
2. inhibit outer hair cell response, possibly affecting the sharpness of mechanical tuning, and thus indirectly affecting inner hair cell response
3. have a latency of 10-30 ms following a stimulus
4. are tonotopically organised
5. permit one cochlea to influence the response of the other (they are only connected via the olivocochlear bundles). Each cochlea can influence the other cochlea's tuning curve (see Pickles, 1998, fig8.5, p242) via the olivocochlear bundles.

Functional significance:-

1. improving the detection of signals in noise. Olivocochlear stimulation suppresses continuous background noise.
2. protection from noise damage. This may be due to changes elicited in the mechanical response of the cochlea
3. controlling the mechanical state of the cochlea. This may be used to adjust for the effects of changes in the cochlea during aging, thus maintaining a relatively constant mechanical state in the cochlea.
4. Attention Some hypotheses suggest that the olivocochlear bundle's ability to change the mechanical state of the cochlea may permit some mechanical control of the tuning of the cochlea thus permitting closer attention to some frequencies at the expense of other frequencies. Presumably, such attentional processes would originate in higher auditory centres. There is little evidence for this hypothesis.

Centrifugal Pathways to the Cochlear Nuclei

The Cochlear Nuclei receive efferent fibres from:-

1. Superior Olivary Complex (the source of the majority of efferent fibres) arising in the pre- and peri-olivary nuclei.
2. Lateral Lemniscus (dorsal and ventral nuclei)
3. Reticular Formation (extends into the pons from the medulla)
4. Inferior Colliculus

Efferent innervation from the Olivary Complex to the cochlear nucleus is both excitatory and inhibitory. There is also evidence that such innervation is both ipsilateral and contralateral.

The main effect of this innervation is enhancement of the detection of a signal in continuous background noise.

Centrifugal Pathways in Higher Centres

A number of descending pathways have been detected:-

1. Auditory Cortex to Medial Geniculate Body (centrifugal fibres terminate on the tonotopically equivalent afferent fibres). This provides a closely coupled loop.
2. Auditory Cortex to various other midbrain nuclei, including the Inferior Colliculus
3. Medial Geniculate Body to Inferior Colliculus
4. Inferior Colliculus to Superior Olivary Complex (most likely to the pre- and peri-olivary nuclei). Note that, evidence for these connections was incomplete at the time Pickles (1988) wrote his book.
5. Inferior Colliculus to Dorsal Cochlear Nucleus

These descending pathways are both inhibitory and excitatory.

Pickles (1988) speculates:-

"We therefore have a system in which reflexes can be established at many levels, and in which the cortex controls the reflexes through descending influences..." (p253)

You can contact me by e-mail at
Robert.Mannell@mq.edu.au