Superior olivary complex

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Superior olivary complex
Gray713.png
Scheme showing the course of the fibers of the lemniscus; medial lemniscus in blue, lateral in red. (Superior olivary nucleus is labeled at center right.)
Details
Identifiers
Latin nucleus olivaris superior
MeSH D065832
NeuroNames 569
NeuroLex ID birnlex_1307
TA98 A14.1.05.415
TA2 5937
FMA 72247
Anatomical terms of neuroanatomy

The superior olivary complex (SOC) or superior olive is a collection of brainstem nuclei that is located in pons, functions in multiple aspects of hearing and is an important component of the ascending and descending auditory pathways of the auditory system. The SOC is intimately related to the trapezoid body: most of the cell groups of the SOC are dorsal (posterior in primates) to this axon bundle while a number of cell groups are embedded in the trapezoid body. Overall, the SOC displays a significant interspecies variation, being largest in bats and rodents and smaller in primates.

Contents

Physiology

The superior olivary nucleus plays a number of roles in hearing. The medial superior olive (MSO) is a specialized nucleus that is believed to measure the time difference of arrival of sounds between the ears (the interaural time difference or ITD). The ITD is a major cue for determining the azimuth of sounds, i.e., localising them on the azimuthal plane – their degree to the left or the right.

The lateral superior olive (LSO) is believed to be involved in measuring the difference in sound intensity between the ears (the interaural level difference or ILD). The ILD is a second major cue in determining the azimuth of high-frequency sounds.

Relationship to auditory system

The superior olivary complex is generally located in the pons, but in humans extends from the rostral medulla to the mid-pons [1] and receives projections predominantly from the anteroventral cochlear nucleus (AVCN) via the trapezoid body, although the posteroventral nucleus projects to the SOC via the intermediate acoustic stria. The SOC is the first major site of convergence of auditory information from the left and right ears. [2]

Primary nuclei

The superior olivary complex is divided into three primary nuclei, the MSO, LSO, and the Medial nucleus of the trapezoid body, and several smaller periolivary nuclei. [3] These three nuclei are the most studied, and therefore best understood. Typically, they are regarded as forming the ascending azimuthal localization pathway.

Medial superior olive (MSO)

The medial superior olive is thought to help locate the azimuth of a sound, that is, the angle to the left or right where the sound source is located. Sound elevation cues are not processed in the olivary complex. The fusiform cells of the dorsal cochlear nucleus (DCN), which are thought to contribute to localization in elevation, bypass the SOC and project directly to the inferior colliculus. Only horizontal data is present, but it does come from two different ear sources, which aids in the localizing of sound on the azimuth axis. [4] The way in which the superior olive does this is by measuring the differences in time between two ear signals recording the same stimulus. Traveling around the head takes about 700 μs, and the medial superior olive is able to distinguish time differences much smaller than this. In fact, it is observed that people can detect interaural differences down to 10 μs. [4] The nucleus is tonotopically organized, but the azimuthal receptive field projection is "most likely a complex, nonlinear map". [5]

The projections of the medial superior olive terminate densely in the ipsilateral central nucleus of the inferior colliculus (CNIC). The majority of these axons are considered to be "round shaped" or type R. These R axons are mostly glutamatergic and contain round synaptic vesicles and form asymmetric synaptic junctions. [2]

Lateral superior olive (LSO)

This olive has similar functions to the medial superior olive, but employs intensity to localize the sound source. [8] The LSO receives excitatory, glutamatergic input from spherical bushy cells in the ipsilateral cochlear nucleus and inhibitory, glycinergic input from the medial nucleus of the trapezoid body (MNTB). The MNTB is driven by excitatory input from globular bushy cells in the contralateral cochlear nucleus. Thus, the LSO receives excitatory input from the ipsilateral ear and inhibitory input from the contralateral ear. This is the basis of ILD sensitivity. Projections from both cochlear nuclei are primarily high frequency, and these frequencies are subsequently represented by the majority of LSO neurons (>2/3 over 2–3 kHz in cat). The LSO does in fact encode frequency across the animals audible range (not just "high" frequency). Additional inputs derive from the ipsilateral LNTB (glycinergic, see below), which provide inhibitory information from the ipsilateral cochlear nucleus. [9] Another possibly inhibitory input derives from ipsilateral AVCN non-spherical cells. These cells are either globular bushy or multipolar (stellate). Either of these two inputs could provide the basis for ipsilateral inhibition seen in response maps flanking the primary excitation, sharpening the unit's frequency tuning. [10] [11]

The LSO projects bilaterally to the central nucleus of the inferior colliculus (ICC). Ipsilateral projections are primarily inhibitory (glycinergic), and the contralateral projections are excitatory. Additional projection targets include the dorsal and ventral nuclei of the lateral lemniscus (DNLL & VNLL). The GABAergic projections from the DNLL form a major source of GABA in the auditory brainstem, and project bilaterally to the ICC and to the contralateral DNLL. These converging excitatory and inhibitory connections may act to decrease the level dependence of ILD sensitivity in the ICC compared to the LSO.

Additional projections form the lateral olivocochlear bundle (LOC), which innervates cochlear inner hair cells. These projections are thought to have a long time constant, and act to normalize the sound level detected by each ear in order to aid in sound localization. [12] Considerable species differences exist: LOC projection neurons are distributed within the LSO in rodents, and surround the LSO in predators (i.e. cat).

Medial nucleus of the trapezoid body (MNTB)

Periolivary nuclei

The SOC is composed of between six and nine periolivary nuclei, depending upon the researcher cited, typically named based upon their location with regard to the primary nuclei. These nuclei surround each of the primary nuclei, and contribute to both the ascending and descending auditory systems. These nuclei also form the source of the olivocochlear bundle, which innervates the cochlea. [16] In the guinea pig, ascending projections to the inferior colliculi are primarily ipsilateral (>80%), with the largest single source coming from the SPON. Also, ventral nuclei (RPO, VMPO, AVPO, & VNTB) are almost entirely ipsilateral, while the remaining nuclei project bilaterally. [17]

NameCatGuinea PigRatMouse
LSOXXXX
MSOXXXX*
MNTBXXXX
LNTBXX"LVPO"X
ALPOXX
PVPOXX
PPOXX"CPO"
VLPOX
DPOXXX
DLPOXX
VTBXX"MVPO"X
AVPOX
VMPOXX
RPOXX
SPN"DMPO"XXX

, [17] *The MSO appears to be smaller and disorganized in mice. [18]

Ventral nucleus of the trapezoid body (VNTB)

Lateral nucleus of the trapezoid body (LNTB)

Superior periolivary nucleus (SPON) (dorsomedial periolivary nucleus (DMPO))

Dorsal periolivary nucleus (DPO)

Dorsolateral periolivary nucleus (DLPO)

Ventrolateral periolivary nucleus (VLPO)

Anterolateral periolivary nucleus (ALPO)

Ventromedial periolivary nucleus (VMPO)

Rostral periolivary nucleus (RPO) (anterior periolivary nucleus (APO))

Caudal periolivary nucleus (CPO) (posterior periolivary nucleus (PPO))

Posteroventral periolivary nucleus (PVPO)

See also

Related Research Articles

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<span class="mw-page-title-main">Auditory system</span> Sensory system used for hearing

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<span class="mw-page-title-main">Lateral lemniscus</span> Brain structure

The lateral lemniscus is a tract of axons in the brainstem that carries information about sound from the cochlear nucleus to various brainstem nuclei and ultimately the contralateral inferior colliculus of the midbrain. Three distinct, primarily inhibitory, cellular groups are located interspersed within these fibers, and are thus named the nuclei of the lateral lemniscus.

<span class="mw-page-title-main">Inferior colliculus</span> Midbrain structure involved in the auditory pathway

The inferior colliculus (IC) is the principal midbrain nucleus of the auditory pathway and receives input from several peripheral brainstem nuclei in the auditory pathway, as well as inputs from the auditory cortex. The inferior colliculus has three subdivisions: the central nucleus, a dorsal cortex by which it is surrounded, and an external cortex which is located laterally. Its bimodal neurons are implicated in auditory-somatosensory interaction, receiving projections from somatosensory nuclei. This multisensory integration may underlie a filtering of self-effected sounds from vocalization, chewing, or respiration activities.

<span class="mw-page-title-main">Pretectal area</span> Structure in the midbrain which mediates responses to ambient light

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<span class="mw-page-title-main">Trapezoid body</span> Part of the auditory pathway

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<span class="mw-page-title-main">Abducens nucleus</span>

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<span class="mw-page-title-main">Koniocellular cell</span> Type of neuron found in the thalamus of primates

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<span class="mw-page-title-main">Medial geniculate nucleus</span>

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<span class="mw-page-title-main">Cochlear nerve</span> Nerve carrying auditory information from the inner ear to the brain

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<span class="mw-page-title-main">Vestibulospinal tract</span> Neural tract in the central nervous system

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<span class="mw-page-title-main">Cochlear nucleus</span> Two cranial nerve nuclei of the human brainstem

The cochlear nucleus (CN) or cochlear nuclear complex comprises two cranial nerve nuclei in the human brainstem, the ventral cochlear nucleus (VCN) and the dorsal cochlear nucleus (DCN). The ventral cochlear nucleus is unlayered whereas the dorsal cochlear nucleus is layered. Auditory nerve fibers, fibers that travel through the auditory nerve carry information from the inner ear, the cochlea, on the same side of the head, to the nerve root in the ventral cochlear nucleus. At the nerve root the fibers branch to innervate the ventral cochlear nucleus and the deep layer of the dorsal cochlear nucleus. All acoustic information thus enters the brain through the cochlear nuclei, where the processing of acoustic information begins. The outputs from the cochlear nuclei are received in higher regions of the auditory brainstem.

<span class="mw-page-title-main">Dorsal cochlear nucleus</span>

The dorsal cochlear nucleus is a cortex-like structure on the dorso-lateral surface of the brainstem. Along with the ventral cochlear nucleus (VCN), it forms the cochlear nucleus (CN), where all auditory nerve fibers from the cochlea form their first synapses.

<span class="mw-page-title-main">Interaural time difference</span> Difference in time that it takes a sound to travel between two ears

The interaural time difference when concerning humans or animals, is the difference in arrival time of a sound between two ears. It is important in the localization of sounds, as it provides a cue to the direction or angle of the sound source from the head. If a signal arrives at the head from one side, the signal has further to travel to reach the far ear than the near ear. This pathlength difference results in a time difference between the sound's arrivals at the ears, which is detected and aids the process of identifying the direction of sound source.

Binaural fusion or binaural integration is a cognitive process that involves the combination of different auditory information presented binaurally, or to each ear. In humans, this process is essential in understanding speech as one ear may pick up more information about the speech stimuli than the other.

<span class="mw-page-title-main">Ventral cochlear nucleus</span>

In the ventral cochlear nucleus (VCN), auditory nerve fibers enter the brain via the nerve root in the VCN. The ventral cochlear nucleus is divided into the anterior ventral (anteroventral) cochlear nucleus (AVCN) and the posterior ventral (posteroventral) cochlear nucleus (PVCN). In the VCN, auditory nerve fibers bifurcate, the ascending branch innervates the AVCN and the descending branch innervates the PVCN and then continue to the dorsal cochlear nucleus. The orderly innervation by auditory nerve fibers gives the AVCN a tonotopic organization along the dorsoventral axis. Fibers that carry information from the apex of the cochlea that are tuned to low frequencies contact neurons in the ventral part of the AVCN; those that carry information from the base of the cochlea that are tuned to high frequencies contact neurons in the dorsal part of the AVCN. Several populations of neurons populate the AVCN. Bushy cells receive input from auditory nerve fibers through particularly large endings called end bulbs of Held. They contact stellate cells through more conventional boutons.

<span class="mw-page-title-main">Calyx of Held</span>

The Calyx of Held is a particularly large synapse in the mammalian auditory central nervous system, so named after Hans Held who first described it in his 1893 article Die centrale Gehörleitung because of its resemblance to the calyx of a flower. Globular bushy cells in the anteroventral cochlear nucleus (AVCN) send axons to the contralateral medial nucleus of the trapezoid body (MNTB), where they synapse via these calyces on MNTB principal cells. These principal cells then project to the ipsilateral lateral superior olive (LSO), where they inhibit postsynaptic neurons and provide a basis for interaural level detection (ILD), required for high frequency sound localization. This synapse has been described as the largest in the brain.

The olivocochlear system is a component of the auditory system involved with the descending control of the cochlea. Its nerve fibres, the olivocochlear bundle (OCB), form part of the vestibulocochlear nerve, and project from the superior olivary complex in the brainstem (pons) to the cochlea.

<span class="mw-page-title-main">Anatomy of the cerebellum</span> Structures in the cerebellum, a part of the brain

The anatomy of the cerebellum can be viewed at three levels. At the level of gross anatomy, the cerebellum consists of a tightly folded and crumpled layer of cortex, with white matter underneath, several deep nuclei embedded in the white matter, and a fluid-filled ventricle in the middle. At the intermediate level, the cerebellum and its auxiliary structures can be broken down into several hundred or thousand independently functioning modules or compartments known as microzones. At the microscopic level, each module consists of the same small set of neuronal elements, laid out with a highly stereotyped geometry.

Bushy cells are two types of second order neuron found in the anterior part of the ventral cochlear nucleus, the AVCN. They can be globular or spherical giving outputs to different parts of the superior olivary complex.

References

PD-icon.svgThis article incorporates text in the public domain from page 787 of the 20th edition of Gray's Anatomy (1918)

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  25. ↑ Friauf E, Ostwald J (1988). "Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase". Experimental Brain Research. 73 (2): 263–284. doi:10.1007/BF00248219. PMID   3215304. S2CID   15155852.
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  28. ↑ White JS, Warr WB (September 1983). "The dual origins of the olivocochlear bundle in the albino rat". The Journal of Comparative Neurology. 219 (2): 203–214. doi:10.1002/cne.902190206. PMID   6619338. S2CID   44291925.
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  33. ↑ Spirou GA, Berrebi AS (April 1996). "Organization of ventrolateral periolivary cells of the cat superior olive as revealed by PEP-19 immunocytochemistry and Nissl stain". The Journal of Comparative Neurology. 368 (1): 100–120. doi: 10.1002/(SICI)1096-9861(19960422)368:1<100::AID-CNE7>3.0.CO;2-7 . PMID   8725296.
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