Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat
Previous electron microscopic studies of synaptic terminal distributions in the lateral geniculate nucleus have been flawed by potential sampling biases favoring larger synapses. We have thus re‐investigated this in the geniculate A‐laminae of the cat with an algorithm to correct this sampling bias....
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Published in: | Journal of comparative neurology (1911) Vol. 416; no. 4; pp. 509 - 520 |
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Abstract | Previous electron microscopic studies of synaptic terminal distributions in the lateral geniculate nucleus have been flawed by potential sampling biases favoring larger synapses. We have thus re‐investigated this in the geniculate A‐laminae of the cat with an algorithm to correct this sampling bias. We used serial reconstructions with the electron microscope to determine the size of each terminal and synaptic type. We observed that RL (retinal) terminals are largest, F (local, GABAergic, inhibitory) terminals are intermediate in size, and RS (cortical and brainstem) terminals are smallest. We also found that synapses from RL terminals are largest, and thus most oversampled, and we used synaptic size data to correct for sampling errors. Doing so, we found that the relative synaptic percentages overall are 11.7% for RL terminals, 27.5% for F, and 60.8% for RS. Furthermore, we distinguished between relay cells and interneurons with post‐embedding immunocytochemistry for GABA (relay cells are GABA negative and interneurons are GABA positive). Onto relay cells, RL terminals contributed 7.1%, F terminals contributed 30.9%, and RS terminals contributed 62.0%. Onto interneurons, RL terminals contributed 48.7%, F terminals contributed 24.4%, and RS terminals contributed 26.9%. We also found that RL terminals included many more separate synaptic contact zones (9.1 ± 1.6) than did F terminals (2.6 ± 0.2) or RS terminals (1.02 ± 0.02). We used these data plus the calculation of overall percentages of each synaptic type to compute the relative percentage of each terminal type in the neuropil: RL terminals represent 1.8%, F terminals represent 14.5%, and RS terminals represent 83.7%. We argue that this relative synaptic paucity is typical for driver inputs (from retina), whereas modulator inputs (all others) require many more synapses to achieve their function. J. Comp. Neurol. 416:509–520, 2000. |
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AbstractList | Previous electron microscopic studies of synaptic terminal distributions in the lateral geniculate nucleus have been flawed by potential sampling biases favoring larger synapses. We have thus re‐investigated this in the geniculate A‐laminae of the cat with an algorithm to correct this sampling bias. We used serial reconstructions with the electron microscope to determine the size of each terminal and synaptic type. We observed that RL (retinal) terminals are largest, F (local, GABAergic, inhibitory) terminals are intermediate in size, and RS (cortical and brainstem) terminals are smallest. We also found that synapses from RL terminals are largest, and thus most oversampled, and we used synaptic size data to correct for sampling errors. Doing so, we found that the relative synaptic percentages overall are 11.7% for RL terminals, 27.5% for F, and 60.8% for RS. Furthermore, we distinguished between relay cells and interneurons with post‐embedding immunocytochemistry for GABA (relay cells are GABA negative and interneurons are GABA positive). Onto relay cells, RL terminals contributed 7.1%, F terminals contributed 30.9%, and RS terminals contributed 62.0%. Onto interneurons, RL terminals contributed 48.7%, F terminals contributed 24.4%, and RS terminals contributed 26.9%. We also found that RL terminals included many more separate synaptic contact zones (9.1 ± 1.6) than did F terminals (2.6 ± 0.2) or RS terminals (1.02 ± 0.02). We used these data plus the calculation of overall percentages of each synaptic type to compute the relative percentage of each terminal type in the neuropil: RL terminals represent 1.8%, F terminals represent 14.5%, and RS terminals represent 83.7%. We argue that this relative synaptic paucity is typical for driver inputs (from retina), whereas modulator inputs (all others) require many more synapses to achieve their function. J. Comp. Neurol. 416:509–520, 2000. Previous electron microscopic studies of synaptic terminal distributions in the lateral geniculate nucleus have been flawed by potential sampling biases favoring larger synapses. We have thus re-investigated this in the geniculate A-laminae of the cat with an algorithm to correct this sampling bias. We used serial reconstructions with the electron microscope to determine the size of each terminal and synaptic type. We observed that RL (retinal) terminals are largest, F (local, GABAergic, inhibitory) terminals are intermediate in size, and RS (cortical and brainstem) terminals are smallest. We also found that synapses from RL terminals are largest, and thus most oversampled, and we used synaptic size data to correct for sampling errors. Doing so, we found that the relative synaptic percentages overall are 11.7% for RL terminals, 27.5% for F, and 60.8% for RS. Furthermore, we distinguished between relay cells and interneurons with post-embedding immunocytochemistry for GABA (relay cells are GABA negative and interneurons are GABA positive). Onto relay cells, RL terminals contributed 7.1%, F terminals contributed 30.9%, and RS terminals contributed 62.0%. Onto interneurons, RL terminals contributed 48.7%, F terminals contributed 24.4%, and RS terminals contributed 26.9%. We also found that RL terminals included many more separate synaptic contact zones (9.1 +/- 1.6) than did F terminals (2.6 +/- 0.2) or RS terminals (1.02 +/- 0.02). We used these data plus the calculation of overall percentages of each synaptic type to compute the relative percentage of each terminal type in the neuropil: RL terminals represent 1.8%, F terminals represent 14.5%, and RS terminals represent 83.7%. We argue that this relative synaptic paucity is typical for driver inputs (from retina), whereas modulator inputs (all others) require many more synapses to achieve their function. |
Author | Van Horn, Susan C. Erişir, Alev Sherman, S. Murray |
Author_xml | – sequence: 1 givenname: Susan C. surname: Van Horn fullname: Van Horn, Susan C. organization: Department of Neurobiology, State University of New York, Stony Brook, New York 11794-5230 – sequence: 2 givenname: Alev surname: Erişir fullname: Erişir, Alev organization: Department of Neurobiology, State University of New York, Stony Brook, New York 11794-5230 – sequence: 3 givenname: S. Murray surname: Sherman fullname: Sherman, S. Murray email: s.sherman@sunysb.edu organization: Department of Neurobiology, State University of New York, Stony Brook, New York 11794-5230 |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/10660881$$D View this record in MEDLINE/PubMed |
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Cites_doi | 10.1113/jphysiol.1985.sp015899 10.1016/0959-4388(94)90058-2 10.1152/jn.1996.76.3.1367 10.1113/jphysiol.1971.sp009581 10.1523/JNEUROSCI.07-06-01780.1987 10.1038/26487 10.1002/cne.903480402 10.1093/cercor/3.1.69 10.1073/pnas.94.4.1517 10.1007/BF00321475 10.1002/cne.903340307 10.1523/JNEUROSCI.15-07-04868.1995 10.1098/rspb.1984.0042 10.1002/(SICI)1096-9861(19980112)390:2<247::AID-CNE7>3.0.CO;2-1 10.1007/BF00228950 10.1016/S0959-4388(96)80052-3 10.1002/cne.901930115 10.1016/S0166-2236(96)10070-9 10.1007/BF00321474 10.1177/40.7.1376741 10.1073/pnas.95.12.7121 10.1007/978-1-4684-4433-9 10.1002/cne.903410105 10.1152/physrev.1982.62.2.738 |
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Erişir A, Van Horn SC, Sherman SM. 1998. Distribution of synapses in the lateral geniculate nucleus of the cat: differences between laminae A and A1 and between relay cells and interneurons. J Comp Neurol 390: 247-255. Guillery RW. 1969b. The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z Zellforsch 96: 1-38. Sherman SM, Guillery RW. 1998. On the actions that one nerve cell can have on another: Distinguishing "drivers" from "modulators." Proc Natl Acad Sci USA 95:7121-7126. Stone J. 1983. Parallel processing in the visual system. New York: Plenum Press. Wilson JR, Friedlander MJ, Sherman SM. 1984. Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proc R Soc Lond B 221: 411-436. Grieve KL, Sillito AM. 1995. Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum. J Neurosci 15: 4868-4874. Bickford ME, Günlük AE, Van Horn SC, Sherman SM. 1994. GABAergic projection from the basal forebrain to the visual sector of the thalamic reticular nucleus in the cat. J Comp Neurol 348: 481-510. Ferster D. 1987. Origin of orientation-selective EPSPs in simple cells of cat visual cortex. J Neurosci 7: 1780-1791. Reid RC, Alonso JM. 1996. The processing and encoding of information in the visual cortex. Curr Opin Neurobiol 6: 475-480. Lisman JE. 1997. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43. Sherman SM, Guillery RW. 1996. The functional organization of thalamocortical relays. J Neurophysiol 76: 1367-1395. Tsumoto T, Suda K. 1980. Three groups of cortico-geniculate neurons and their distribution in binocular and monocular segments of cat striate cortex. 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References_xml | – volume: 334 start-page: 410 year: 1993 end-page: 430 article-title: Evidence that cholinergic axons from the parabrachial region of the brainstem are the exclusive source of nitric oxide in the lateral geniculate nucleus of the cat publication-title: J Comp Neurol – volume: 40 start-page: 1011 year: 1992 end-page: 1020 article-title: Techniques to optimize post‐embedding single and double staining for amino acid neurotransmitters publication-title: J Histochem Cytochem – year: 1983 – volume: 390 start-page: 247 year: 1998 end-page: 255 article-title: Distribution of synapses in the lateral geniculate nucleus of the cat: differences between laminae A and A1 and between relay cells and interneurons publication-title: J Comp Neurol – volume: 369 start-page: 249 year: 1985 end-page: 268 article-title: A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them publication-title: J Physiol (Lond) – volume: 4 start-page: 563 year: 1994 end-page: 568 article-title: Linearity of synaptic interactions in the assembly of receptive fields in cat visual cortex publication-title: Curr Opin Neurobiol – volume: 96 start-page: 1 year: 1969b end-page: 38 article-title: The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat publication-title: Z Zellforsch – volume: 86 start-page: 257 year: 1991 end-page: 270 article-title: A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus publication-title: Exp Brain Res – volume: 193 start-page: 223 year: 1980 end-page: 236 article-title: Three groups of cortico‐geniculate neurons and their distribution in binocular and monocular segments of cat striate cortex publication-title: J Comp Neurol – volume: 6 start-page: 475 year: 1996 end-page: 480 article-title: The processing and encoding of information in the visual cortex publication-title: Curr Opin Neurobiol – start-page: 289 year: 1998 end-page: 328 – volume: 395 start-page: 384 year: 1998 end-page: 387 article-title: Paired‐spike interactions and synaptic efficacy of retinal inputs to the thalamus publication-title: Nature – volume: 341 start-page: 39 year: 1994 end-page: 49 article-title: Polyneuronal innervation of spiny stellate neurons in cat visual cortex publication-title: J Comp Neurol – volume: 95 start-page: 7121 year: 1998 end-page: 7126 article-title: On the actions that one nerve cell can have on another: Distinguishing “drivers” from “modulators.” publication-title: Proc Natl Acad Sci USA – volume: 20 start-page: 38 year: 1997 end-page: 43 article-title: Bursts as a unit of neural information: making unreliable synapses reliable publication-title: Trends Neurosci – volume: 217 start-page: 473 year: 1971 end-page: 496 article-title: Sustained and transient neurones in the cat's retina and lateral geniculate nucleus publication-title: J Physiol (Lond) – volume: 96 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Snippet | Previous electron microscopic studies of synaptic terminal distributions in the lateral geniculate nucleus have been flawed by potential sampling biases... |
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SubjectTerms | Algorithms Animals Cats - anatomy & histology gamma-Aminobutyric Acid - metabolism Geniculate Bodies - metabolism Geniculate Bodies - ultrastructure Image Processing, Computer-Assisted Immunohistochemistry interneurons Microscopy, Electron Nerve Endings - metabolism Nerve Endings - ultrastructure relay cells sensory transmission Synapses - ultrastructure synaptic terminals thalamus |
Title | Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat |
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