Superior olivary complex

For the cerebellar structure, see Dentate nucleus.
Brain: Superior olivary complex
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.)
Latin nucleus olivaris superior
Gray's subject #187 787
NeuroLex ID birnlex_1307

The superior olivary complex (or SOC or superior olive) is a collection of brainstem nuclei that functions in multiple aspects of hearing and is an important component of the ascending and descending auditory pathways. 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 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 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 human extends from the rostral medulla to the mid-pons[1] and receives projections predominantly from the anteroventral cochlear nucleus 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. One’s first instincts may be to think that this nucleus includes vertical information, but this is not the case; the information processed in the MSO is restricted to the horizontal plane. The fusiform cells of the Dorsal cochlear nucleus, 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 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 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. 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 2-3kHz in cat). It should be noted that 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 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]

Name Cat Guinea Pig Rat Mouse
LSO X X X X
MSO X X X X
MNTB X X X X
LNTB X X "LVPO" X
ALPO X X
PVPO X X
PPO X X "CPO"
VLPO X
DPO X X X
DLPO X X
VTB X X "MVPO" X
AVPO X
VMPO X X
RPO X X
SPN "DMPO" X X X

[17]

Ventral Nucleus of Trapezoid Body (VNTB)

Lateral Nucleus of the Trapezoid Body (LNTB)

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

Dorsal Periolivary Nucleus (DPO)

[29]

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)

Pathophysiology

An autopsy of a 21-year-old woman with autism, epilepsy and mental retardation found a near-complete absence of the superior olive.[30]

See also

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 Kandel, et al. Principles of Neural Science. Fourth ed. pp 591-624. Copyright 2000, by McGraw-Hill Co.
  5. ^ Oliver, Douglas L. et al. Topography of Interaural Temporal Disparity Coding in Projections of Medial Superior Olive to Inferior Colliculus. The Journal of Neuroscience, August 13, 2003, 23(19):7438-7449
  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. ^ Kulesza et al., (2011) Malformation of the human superior olive in autistic spectrum disorders. Brain Res. 2011 Jan 7;1367:360-71.
  8. ^ 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.
  9. ^ a b c Glendenning, K. K., R. B. Masterton, et al. (1991). "Acoustic chiasm. III: Nature, distribution, and sources of afferents to the lateral superior olive in the cat." J Comp Neurol 310(3): 377-400.
  10. ^ 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.
  11. ^ Brownell, W. E., P. B. Manis, et al. (1979). "Ipsilateral inhibitory responses in the cat lateral superior olive." Brain Res 177(1): 189-93.
  12. ^ Darrow, K. N., S. F. Maison, et al. (2006). "Cochlear efferent feedback balances interaural sensitivity." Nat Neurosci 9(12): 1474-6.
  13. ^ Bazwinsky et al., Characterization of the rhesus monkey superior olivary complex by calcium binding proteins and synaptophysin.J Anat. 2005 Dec;207(6):745-61.
  14. ^ Bazwinsky et al., Characterization of the human superior olivary complex by calcium binding proteins and neurofilament H (SMI-32).J Comp Neurol. 2003 Feb 10;456(3):292-303.
  15. ^ Kulesza, Cytoarchitecture of the human superior olivary complex: nuclei of the trapezoid body and posterior tier.Hear Res. 2008 Jul;241(1-2):52-63. Epub 2008 May 10.
  16. ^ 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.
  17. ^ 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.
  18. ^ 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.
  19. ^ 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.
  20. ^ 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.
  21. ^ 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.
  22. ^ Wenthold, R. J., D. Huie, et al. (1987). "Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex." Neuroscience 22(3): 897-912.
  23. ^ 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.
  24. ^ 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.
  25. ^ 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.
  26. ^ 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.
  27. ^ WHITE JS, WARR WB. The dual origins of the olivocochlear bundle in the albino rat. J. Comp. Neurol. 219:203–214, 1983.
  28. ^ 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.
  29. ^ Tsuchitani, C. (1977). "Functional organization of lateral cell groups of cat superior olivary complex." J Neurophysiol 40(2): 296-318.
  30. ^ 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. doi:10.1002/(SICI)1096-9861(19960624)370:2<247::AID-CNE8>3.0.CO;2-2. PMID 8808733. 

External links

This article was originally based on an entry from a public domain edition of Gray's Anatomy. As such, some of the information contained within it may be outdated.

Dorsal/
(tegmentum)
Surface
White: Sensory/ascending
White: Motor/descending
Other grey
Ventral/
(base)
White: Motor/descending
Surface
Other grey: Raphe/
reticular

M: CNS

anat(n/s/m/p/4/e/b/d/c/a/f/l/g)/phys/devp

noco(m/d/e/h/v/s)/cong/tumr, sysi/epon, injr

proc, drug(N1A/2AB/C/3/4/7A/B/C/D)
Auditory and vestibular pathways
Auditory
Vestibular

M: EAR

anat(e/p)/phys/devp

noco/cong, epon

proc, drug(S2)