Superior olivary complex

The superior olivary nucleus (or superior olivary complex, SOC or superior olive) is a small mass of gray substance situated on the dorsal surface of the lateral part of the trapezoid body. Small in humans, but well developed in certain animals, it exhibits the similar structure as the inferior olivary nucleus, and is situated immediately above it. Some of the fibers of the trapezoid body end by arborizing around the cells of this nucleus, while others arise from these cells.

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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 low frequency 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 level difference of sounds 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 human extends from the rostral medulla to the mid-pons^[1] and receives projections predominantly from the anteroventral cochlear nucleus via the ventral acoustic stria, although the posteroventral nucleus projects there as well via the intermediate acoustic stria. It is at this site where the first major binaural interactions occur.^[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 position of a sound on the azimuth axis.^[4] The azimuth axis is the angle from a certain direction, ie: 32 degrees from north. One’s first instincts may be to think that this nucleus includes vertical information, but this is not the case. The fusiform cells do not project to anything in the level of the pons, and only come into play at 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.^[5] 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 it is assumed that the medial superior olive is able to detect this. In fact, it is observed that people can detect interaural differences down to 10 microseconds.^[5] The nucleus is tonotopically organized, but the azimuthal receptive field projection is “most likely a complex, nonlinear map.”^[4]

The projections of the ipsilateral medial superior olive terminate densely in the central nucleus of the inferior colliculus. 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]

• This is the largest of the nuclei and in human contains approximately 15,500 neurons ^[6].
• Each MSO receives low-frequency bilateral inputs from the right and left AVCNs.
• The output is to the ipsilateral lateral lemniscus and ultimately to the inferior colliculus.
• The MSO responds better to binaural stimuli.
• Its main function involves detection of differences in arrival time of sounds to the two ears which is part of localization process (ITD).

Lateral superior olive (LSO)

This olive has similar functions to the medial superior olive, but employs intensity to localize the sound source.^[7] This is the part of the brain stem that labels the louder sound from the left ear as being on the left hand side. The lateral olive receives input from both cochlear nuclei, from ipsilateral AVCN spherical bushy cells and contralateral AVCN globular bushy cells via the ipsilateral MNTB. MNTB principal cells are glycinergic, providing a source of inhibition to the LSO, and forming 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 2-3kHz in cat). Additional inputs derive from the ipsilateral LNTB (glycinergic, see below), which provide inhibitory information from the ipsilateral cochlear nucleus^[8]. 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.^[9][10]

The LSO primarily projects, bilaterally, to the central nucleus of the inferior colliculus (ICC). Ipsilateral projections are primarily inhibitory (glycinergic), and contralateral excitatory. Additional projection targets include the Dorsal and Ventral nuclei of the Lateral Lemniscus (DNLL & VNLL). The GABAergic projections from the DNLL form the primary source of GABA in the brainstem auditory system, and project primarily to the contralateral ICC. These converging excitatory and inhibitory connections act to sharpen 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^[11]. 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 Trapezoid Body (MNTB)

• The MNTB is the smallest part of SOC; the presence of the MNTB in the human brainstem is in doubt.
• Each neuron receives only high-frequency input via a Calyx of held from the contralateral AVCN, and its output projects to the ipsilateral LSO.
• There are two response types found: a ‘chopper type’ similar to spindle cells in the AVCN and a primary type which is similar to those of Bushy Cells in the AVCN.

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.^[12] 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.^[13]

Ventral Nucleus of Trapezoid Body (VNTB)

• The VNTB is a small nucleus located laterally to the MNTB, and ventral to the MSO.^[14]
• Comprised of a heterogeneous population of cells, this nucleus projects to many auditory nuclei, and forms the medial olivocochlear bundle (MOC) which innervates cochlear outer hair cells ^[15]. These cells contain electromotile fibers, and act as mechanical amplifiers/attenuators within the cochlea.
• The nucleus projects to both IC, with no cells projecting bilaterally.^[16]

Lateral Nucleus of the Trapezoid Body (LNTB)

• Located ventral to the LSO^[14]
• AVCN spherical bushy cells project collaterals bilaterally, and globular bushy cells project collaterals ipsilaterally to LNTB neurons.^[17]
• Cells are immunoreactive for glycine^[18], and are retrogradely labeled following injection of tritiated glycine into the LSO^[8]
• The nucleus projects to both IC, with few cells projecting bilaterally^[16], as well as the ipsilateral LSO^[8].
• Large multipolar cells project to the cochlear nucleus, but not the IC, in both cat and guinea pig.^[16][19]
• Inputs are often via end-bulbs of held, producing very fast signal transduction.

Superior Periolivary Nucleus (SPON) (Dorsomedial Periolivary Nucleus (DMPO))

• Located directly dorsal to the MNTB^[14]
• In rat, SPON is a homogeneous GABAergic nucleus. These tonotopically organized neurons receive excitatory inputs from octopus and multipolar cells in the contralateral ventral cochlear nucleus^[20], a glycinergic (inhibitory) input from the ipsilateral MNTB, an unknown GABAergic (inhibitory) input, and project to the ipsilateral ICC.^[21] Most neurons respond only at the offset of a stimulus, can phase lock to AM stimuli up to 200 Hz, and may form the basis for ICC duration selectivity.^[22] Notably, SPON neurons do not receive descending inputs from the IC, and it does not project to the cochlea or cochlear nucleus as many periolivary nuclei do.^[23]
• In guinea pig, round to oval multipolar cells project to both IC, with many cells projecting bilaterally. The more elongated cells that project to the cochlear nucleus to not project to the ICC. There appear to be to populations of cells, one that projects ipsilaterally, and one that projects bilaterally.^[16]
• The majority of information had come from rodent SPON, due to the nucleus' prominent size in these species, with very few studies have been done in cat DMPO^[24], none of which were extensive.

Dorsal Periolivary Nucleus (DPO)

• Located dorsal and medial to the LSO^[14]
• Contains both EE (excited by both ears) and E0 (excited by the contralateral ear only) units.
• Neurons are tonotopically organized, and high frequency.
• May belong to a single nucleus along with the DLPO

^[25]

• The nucleus projects to both IC, with no cells projecting bilaterally.^[16]

Dorsolateral Periolivary Nucleus (DLPO)

• Located dorsal and lateral to the LSO^[14]
• Contains both EE (excited by both ears) and E0 (excited by the contralateral ear only) units.
• Neurons are tonotopically organized, and low frequency.
• May belong to a single nucleus along with the DPO
• The nucleus projects to both IC, with few cells projecting bilaterally.^[16]

Ventrolateral Periolivary Nucleus (VLPO)

• Located ventral to and within the ventral hillus of the LSO^[14]
• Contains both EI (excited by contralateral and inhibited by ipsilateral ear) and E0 (excited by the contralateral ear only) units.
• Neurons are tonotopically organized, and high frequency.

Anterolateral Periolivary Nucleus (ALPO)

• The nucleus projects to both IC, with no cells projecting bilaterally.^[16]
• Large multipolar cells project to the cochlear nucleus, but not the IC, in both cat and guinea pig.^[16][19]

Ventromedial Periolivary Nucleus (VMPO)

• Located between the MSO and MNTB.^[14]
• Sends projections to the ICC bilaterally.^[16]
• The nucleus projects to both IC, with no cells projecting bilaterally.^[16]

Rostral Periolivary Nucleus (RPO) (Anterior Periolivary Nucleus (APO))

• Located between the rostral pole of the MSO and the VNLL^[14]

Caudal Periolivary Nucleus (CPO) (Posterior Periolivary Nucleus (PPO))

• Located between the caudal pole of the MSO and the facial nucleus (7N)^[14]

Posteroventral Periolivary Nucleus (PVPO)

• The nucleus projects to both IC, with no cells projecting bilaterally.^[16]

Pathophysiology

An autopsy of a 21-year-old woman with autism, epilepsy and mental retardation found a near-complete absence of the superior olive.^[26]

See also

• Olivary body

References

1. ^ Kulesza RJ, Cytoarchitecture of the human superior olivary complex: Medial and lateral superior olive. Hearing Research 225(2007) 80-90
2. ^ ^{a b} Oliver DL, et al. Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography. J Comp Neurol. 1995 Sep 11;360(1):17-32
3. ^ Cajal, S. R. Y. and L. Azoulay (1909). Histologie du système nerveux de l'homme et des vertébrés. Paris, Maloine.
4. ^ ^{a b}
5. ^ ^{a b} Kandel, et al Principles of Neuroscience. Fourth ed. pp 591-624. Copyright 2000, by McGraw-Hill Co.
6. ^ Kulesza, R. J., Jr. (2007). "Cytoarchitecture of the human superior olivary complex: medial and lateral superior olive." Hear Res 225(1-2): 80-90.
7. ^ Tsuchitani, C. and J. C. Boudreau (1967). "Encoding of stimulus frequency and intensity by cat superior olive S-segment cells." J Acoust Soc Am 42(4): 794-805.
8. ^ ^{a b c}
9. ^ Wu, S. H. and J. B. Kelly (1994). "Physiological evidence for ipsilateral inhibition in the lateral superior olive: synaptic responses in mouse brain slice." Hear Res 73(1): 57-64.
10. ^ Brownell, W. E., P. B. Manis, et al. (1979). "Ipsilateral inhibitory responses in the cat lateral superior olive." Brain Res 177(1): 189-93.
11. ^ Darrow, K. N., S. F. Maison, et al. (2006). "Cochlear efferent feedback balances interaural sensitivity." Nat Neurosci 9(12): 1474-6.
12. ^ Warr, W. B. and J. J. Guinan, Jr. (1979). "Efferent innervation of the organ of corti: two separate systems." Brain Res 173(1): 152-5.
13. ^ ^{a b} Schofield, B. R. and N. B. Cant (1991). "Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology." J Comp Neurol 314(4): 645-70.
14. ^ ^{a b c d e f g h i} Illing, R. B., K. S. Kraus, et al. (2000). "Plasticity of the superior olivary complex." Microsc Res Tech 51(4): 364-81.
15. ^ Warr, W. B. and J. E. Beck (1996). "Multiple projections from the ventral nucleus of the trapezoid body in the rat." Hear Res 93(1-2): 83-101.
16. ^ ^{a b c d e f g h i j k} Schofield, B. R. and N. B. Cant (1992). "Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus." J Comp Neurol 317(4): 438-55.
17. ^ Smith, P. H., P. X. Joris, et al. (1993). "Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive." J Comp Neurol 331(2): 245-60.
18. ^ Wenthold, R. J., D. Huie, et al. (1987). "Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex." Neuroscience 22(3): 897-912.
19. ^ ^{a b} Adams, J. C. (1983). "Cytology of periolivary cells and the organization of their projections in the cat." J Comp Neurol 215(3): 275-89.
20. ^ Friauf, E. and J. Ostwald (1988). "Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase." Exp Brain Res 73(2): 263-84.
21. ^ Kulesza, R. J., Jr. and A. S. Berrebi (2000). "Superior paraolivary nucleus of the rat is a GABAergic nucleus." J Assoc Res Otolaryngol 1(4): 255-69.
22. ^ Kulesza, R. J., Jr., G. A. Spirou, et al. (2003). "Physiological response properties of neurons in the superior paraolivary nucleus of the rat." J Neurophysiol 89(4): 2299-312.
23. ^ WHITE JS, WARR WB. The dual origins of the olivocochlear bundle in the albino rat. J. Comp. Neurol. 219:203–214, 1983.
24. ^ Guinan, J. J., Jr., S. S. Guinan, et al. (1972). "Single auditory units in the superior olivary complex. I. Responses to sounds and classifications based on physiological properties." Int J Neurosci 4: 101-20.
25. ^ Tsuchitani, C. (1977). "Functional organization of lateral cell groups of cat superior olivary complex." J Neurophysiol 40(2): 296-318.
26. ^ Rodier PM, Ingram JL, Tisdale B, Nelson S, Romano J (1996). "Embryological origin for autism: developmental anomalies of the cranial nerve motor nuclei". J Comp Neurol 370 (2): 247–61. PMID 8808733.

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