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Open Access 01-09-2017 | Original Article

Synaptic connections formed by patchy projections of pyramidal cells in the superficial layers of cat visual cortex

Authors: German Koestinger, Kevan A. C. Martin, Stephan Roth, Elisha S. Rusch

Published in: Brain Structure and Function | Issue 7/2017

Abstract

The present study is the first to describe quantitatively the patterns of synaptic connections made by the patchy network of pyramidal cell axons in the superficial layers of cat V1 in relation to the orientation map. Intrinsic signal imaging of the orientation map was combined with 3D morphological reconstructions of physiologically-characterized neurons at light and electron microscope levels. A Similarity Index (SI) expressed the similarity of the orientation domain of a given bouton cluster to that of its parent dendritic tree. Six pyramidal cells whose axons had a wide range of SIs were examined. Boutons were sampled from five local and five distal clusters, and from the linear segments that link the clusters. The synaptic targets were reconstructed by serial section electron microscopy. Of the 233 synapses examined, 182 synapses were formed with spiny neurons, the remainder with smooth neurons. The proportion of smooth neurons that were synaptic targets varied greatly (from 0 to 50%) between the cluster samples, but was not correlated with the SI. The postsynaptic density sizes were similar for synapses in local and distal clusters, regardless of their SI. This heterogeneity in the synaptic targets of single cells within the superficial layers is a network feature well-suited for context-dependent processing.

Anderson JC, Dehay C, Friedlander MJ, Martin KAC, Nelson JC (1992) Synaptic connections of physiologically identified geniculocortical axons in kitten cortical area 17. Proc R Soc B Biol Sci 250(1329):187–194. doi:10.1098/rspb.1992.0148 CrossRef

Anderson JC, Kennedy H, Martin KA (2011) Pathways of attention: synaptic relationships of frontal eye field to V4, lateral intraparietal cortex, and area 46 in macaque monkey. J Neurosci 31(30):10872–10881. doi:10.1523/JNEUROSCI.0622-11.2011 CrossRefPubMed

Angelucci A, Bullier J (2003) Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? J Physiol Paris 97(2–3):141–154. doi:10.1016/j.jphysparis.2003.09.001 CrossRefPubMed

Ben-Shahar O, Zucker S (2004) Geometrical computations explain projection patterns of long-range horizontal connections in visual cortex. Neural Comput 16(3):445–476. doi:10.1162/089976604772744866 CrossRefPubMed

Benucci A, Frazor RA, Carandini M (2007) Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55(1):103–117. doi:10.1016/j.neuron.2007.06.017 CrossRefPubMedPubMedCentral

Binzegger T, Douglas RJ, Martin KA (2004) A quantitative map of the circuit of cat primary visual cortex. J Neurosci 24(39):8441–8453. doi:10.1523/JNEUROSCI.1400-04.2004 CrossRefPubMed

Binzegger T, Douglas RJ, Martin KA (2007) Stereotypical bouton clustering of individual neurons in cat primary visual cortex. J Neurosci 27(45):12242–12254. doi:10.1523/JNEUROSCI.3753-07.200 CrossRefPubMed

Bishop GH, Clare MH, Landau WM (1971) The relation of axon sheath thickness to fiber size in the central nervous system of vertebrates. Int J Neurosci 2(2):69–77CrossRefPubMed

Bishop PO, Coombs JS, Henry GH (1973) Receptive fields of simple cells in the cat striate cortex. J Physiol 231(1):31–60CrossRefPubMedPubMedCentral

Bock DD, Lee WC, Kerlin AM, Andermann ML, Hood G, Wetzel AW, Yurgenson S, Soucy ER, Kim HS, Reid RC (2011) Network anatomy and in vivo physiology of visual cortical neurons. Nature 471(7337):177–182. doi:10.1038/nature09802 CrossRefPubMedPubMedCentral

Bonhoeffer T, Grinvald A (1996) Optical imaging based on intrinsic signals: the methodology. In: Toga AW, Mazziotta JC (eds) Brain mapping: the methods. Academic Press, Amsterdam, pp 55–97

Bopp R, Macarico da Costa N, Kampa BM, Martin KA, Roth MM (2014) Pyramidal cells make specific connections onto smooth (GABAergic) neurons in mouse visual cortex. PLoS Biol 12(8):e1001932. doi:10.1371/journal.pbio.1001932 CrossRefPubMedPubMedCentral

Bosking WH, Zhang Y, Schofield B, Fitzpatrick D (1997) Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J Neurosci 17(6):2112–2127PubMed

Braitenberg V, Schüz A (1991) Anatomy of the cortex: statistics and geometry. Studies of brain function, vol 18. Springer, Berlin

Bringuier V, Chavane F, Glaeser L, Fregnac Y (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283(5402):695–699CrossRefPubMed

Buzas P, Kovacs K, Ferecsko AS, Budd JM, Eysel UT, Kisvarday ZF (2006) Model-based analysis of excitatory lateral connections in the visual cortex. J Comp Neurol 499(6):861–881. doi:10.1002/cne.21134 CrossRefPubMed

Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S, Longair M, Tomancak P, Hartenstein V, Douglas RJ (2012) TrakEM2 software for neural circuit reconstruction. PLoS One 7(6):e38011. doi:10.1371/journal.pone.0038011 CrossRefPubMedPubMedCentral

Chisum HJ, Mooser F, Fitzpatrick D (2003) Emergent properties of layer 2/3 neurons reflect the collinear arrangement of horizontal connections in tree shrew visual cortex. J Neurosci 23(7):2947–2960PubMed

Chomiak T, Hu B (2009) What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PLoS One 4(11):e7754. doi:10.1371/journal.pone.0007754 CrossRefPubMedPubMedCentral

Cohen MR, Kohn A (2011) Measuring and interpreting neuronal correlations. Nat Neurosci 14(7):811–819. doi:10.1038/nn.2842 CrossRefPubMedPubMedCentral

Cossell L, Iacaruso MF, Muir DR, Houlton R, Sader EN, Ko H, Hofer SB, Mrsic-Flogel TD (2015) Functional organization of excitatory synaptic strength in primary visual cortex. Nature 518(7539):399–403. doi:10.1038/nature14182 CrossRefPubMedPubMedCentral

Crook JM, Kisvarday ZF, Eysel UT (1997) GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity. Vis Neurosci 14(1):141–158CrossRefPubMed

Crook JM, Kisvarday ZF, Eysel UT (1998) Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques. Eur J Neurosci 10(6):2056–2075CrossRefPubMed

da Costa NM, Hepp K, Martin KA (2009) A systematic random sampling scheme optimized to detect the proportion of rare synapses in the neuropil. J Neurosci Methods 180(1):77–81. doi:10.1016/j.jneumeth.2009.03.001 CrossRefPubMed

Douglas RJ, Martin KA (1991) A functional microcircuit for cat visual cortex. J Physiol 440:735–769CrossRefPubMedPubMedCentral

Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27:419–451. doi:10.1146/annurev.neuro.27.070203.144152 CrossRefPubMed

Douglas RJ, Martin KAC, Whitteridge D (1989) A canonical microcircuit for neocortex. Neural Comput 1(4):480–488. doi:10.1162/neco.1989.1.4.480 CrossRef

Dragoi V, Sharma J, Sur M (2000) Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28(1):287–298CrossRefPubMed

Dragoi V, Rivadulla C, Sur M (2001) Foci of orientation plasticity in visual cortex. Nature 411(6833):80–86. doi:10.1038/35075070 CrossRefPubMed

Engel AK, Konig P, Gray CM, Singer W (1990) Stimulus-dependent neuronal oscillations in cat visual cortex: inter-columnar interaction as determined by cross-correlation analysis. Eur J Neurosci 2(7):588–606CrossRefPubMed

Felsen G, Shen YS, Yao H, Spor G, Li C, Dan Y (2002) Dynamic modification of cortical orientation tuning mediated by recurrent connections. Neuron 36(5):945–954CrossRefPubMed

Field DJ, Hayes A, Hess RF (1993) Contour integration by the human visual system: evidence for a local “association field”. Vis Res 33(2):173–193CrossRefPubMed

Fournier J, Monier C, Levy M, Marre O, Sari K, Kisvarday ZF, Fregnac Y (2014) Hidden complexity of synaptic receptive fields in cat V1. J Neurosci 34(16):5515–5528. doi:10.1523/JNEUROSCI.0474-13.2014 CrossRefPubMed

Gilbert CD, Wiesel TN (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9(7):2432–2442PubMed

Gilbert CD, Wiesel TN (1992) Receptive field dynamics in adult primary visual cortex. Nature 356(6365):150–152. doi:10.1038/356150a0 CrossRefPubMed

Girardin CC, Martin KA (2009) Inactivation of lateral connections in cat area 17. Eur J Neurosci 29(10):2092–2102. doi:10.1111/j.1460-9568.2009.06752.x CrossRefPubMed

Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86(5):1698–1702CrossRefPubMedPubMedCentral

Gray CM, Engel AK, Konig P, Singer W (1990) Stimulus-dependent neuronal oscillations in cat visual cortex: receptive field properties and feature dependence. Eur J Neurosci 2(7):607–619CrossRefPubMed

Grinvald A, Lieke EE, Frostig RD, Hildesheim R (1994) Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J Neurosci 14(5 Pt 1):2545–2568PubMed

Hirsch JA, Gilbert CD (1991) Synaptic physiology of horizontal connections in the cat’s visual cortex. J Neurosci 11(6):1800–1809PubMed

Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154CrossRefPubMedPubMedCentral

Hubel DH, Wiesel TN (1965) Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J Neurophysiol 28:229–289PubMed

Hursh JB (1939) Conduction velocity and diameter of nerve fibers. Am J Physiol 127(1):131–139

Karube F, Kisvarday ZF (2011) Axon topography of layer IV spiny cells to orientation map in the cat primary visual cortex (area 18). Cereb Cortex 21(6):1443–1458. doi:10.1093/cercor/bhq232 CrossRefPubMed

Keller AJ, Martin KA (2015) Local circuits for contrast normalization and adaptation investigated with two-photon imaging in cat primary visual cortex. J Neurosci 35(27):10078–10087. doi:10.1523/JNEUROSCI.0906-15.2015 CrossRefPubMed

Kisvarday ZF, Martin KA, Freund TF, Magloczky Z, Whitteridge D, Somogyi P (1986) Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Exp Brain Res 64(3):541–552CrossRefPubMed

Lee WC, Bonin V, Reed M, Graham BJ, Hood G, Glattfelder K, Reid RC (2016) Anatomy and function of an excitatory network in the visual cortex. Nature 532(7599):370–374. doi:10.1038/nature17192 CrossRefPubMedPubMedCentral

LeVay S (1988) Patchy intrinsic projections in visual cortex, area 18, of the cat: morphological and immunocytochemical evidence for an excitatory function. J Comp Neurol 269(2):265–274. doi:10.1002/cne.902690210 CrossRefPubMed

Levitt JB, Lewis DA, Yoshioka T, Lund JS (1993) Topography of pyramidal neuron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46). J Comp Neurol 338(3):360–376. doi:10.1002/cne.903380304 CrossRefPubMed

Malach R, Tootell RB, Malonek D (1994) Relationship between orientation domains, cytochrome oxidase stripes, and intrinsic horizontal connections in squirrel monkey area V2. Cereb Cortex 4(2):151–165CrossRefPubMed

Martin KA (1988) The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol 73(5):637–702CrossRefPubMed

Martin KA, Schroder S (2013) Functional heterogeneity in neighboring neurons of cat primary visual cortex in response to both artificial and natural stimuli. J Neurosci 33(17):7325–7344. doi:10.1523/JNEUROSCI.4071-12.2013 CrossRefPubMed

Martin KA, Whitteridge D (1984a) Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. J Physiol 353:463–504CrossRefPubMedPubMedCentral

Martin KA, Whitteridge D (1984b) The relationship of receptive field properties to the dendritic shape of neurones in the cat striate cortex. J Physiol 356:291–302CrossRefPubMedPubMedCentral

Martin KA, Roth S, Rusch ES (2014a) Superficial layer pyramidal cells communicate heterogeneously between multiple functional domains of cat primary visual cortex. Nat Commun 5:5252. doi:10.1038/ncomms6252 CrossRefPubMedPubMedCentral

Martin KAC, Roth S, Rusch ES (2014b) Superficial layer pyramidal cells communicate heterogeneously between multiple functional domains of cat primary visual cortex. Nat Commun. doi:10.1038/ncomms6252

McGuire BA, Gilbert CD, Rivlin PK, Wiesel TN (1991) Targets of horizontal connections in macaque primary visual cortex. J Comp Neurol 305(3):370–392. doi:10.1002/cne.903050303 CrossRefPubMed

Monier C, Chavane F, Baudot P, Graham LJ, Fregnac Y (2003) Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37(4):663–680CrossRefPubMed

Morrone MC, Burr DC, Maffei L (1982) Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc R Soc Lond B Biol Sci 216(1204):335–354CrossRefPubMed

Muir DR, Da Costa NM, Girardin CC, Naaman S, Omer DB, Ruesch E, Grinvald A, Douglas RJ (2011) Embedding of cortical representations by the superficial patch system. Cereb Cortex 21(10):2244–2260. doi:10.1093/cercor/bhq290 CrossRefPubMedPubMedCentral

Muller JR, Metha AB, Krauskopf J, Lennie P (1999) Rapid adaptation in visual cortex to the structure of images. Science 285(5432):1405–1408CrossRefPubMed

Phillips CG, Powell TP, Wiesendanger M (1971) Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon’s cortex. J Physiol 217(2):419–446CrossRefPubMedPubMedCentral

Ratzlaff EH, Grinvald A (1991) A tandem-lens epifluorescence macroscope: hundred-fold brightness advantage for wide-field imaging. J Neurosci Methods 36(2–3):127–137CrossRefPubMed

Rockland KS, Lund JS (1982) Widespread periodic intrinsic connections in the tree shrew visual cortex. Science 215(4539):1532–1534CrossRefPubMed

Rushton WA (1951) A theory of the effects of fibre size in medullated nerve. J Physiol 115(1):101–122CrossRefPubMedPubMedCentral

Schmidt KE, Goebel R, Lowel S, Singer W (1997) The perceptual grouping criterion of colinearity is reflected by anisotropies of connections in the primary visual cortex. Eur J Neurosci 9(5):1083–1089CrossRefPubMed

Sillito AM, Grieve KL, Jones HE, Cudeiro J, Davis J (1995) Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378(6556):492–496. doi:10.1038/378492a0 CrossRefPubMed

Sincich LC, Blasdel GG (2001) Oriented axon projections in primary visual cortex of the monkey. J Neurosci 21(12):4416–4426PubMed

Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134(Pt 2):127–136CrossRefPubMed

Stettler DD, Das A, Bennett J, Gilbert CD (2002) Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36(4):739–750CrossRefPubMed

Waxman SG, Bennett MV (1972) Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. Nat New Biol 238(85):217–219CrossRefPubMed

Yao H, Dan Y (2001) Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 32(2):315–323CrossRefPubMed

Yao H, Shen Y, Dan Y (2004) Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning. Proc Natl Acad Sci USA 101(14):5081–5086. doi:10.1073/pnas.0302510101 CrossRefPubMedPubMedCentral

Zariwala HA, Madisen L, Ahrens KF, Bernard A, Lein ES, Jones AR, Zeng H (2011) Visual tuning properties of genetically identified layer 2/3 neuronal types in the primary visual cortex of cre-transgenic mice. Front Syst Neurosci 4:162. doi:10.3389/fnsys.2010.00162 CrossRefPubMedPubMedCentral

Title: Synaptic connections formed by patchy projections of pyramidal cells in the superficial layers of cat visual cortex
Authors: German Koestinger
Kevan A. C. Martin
Stephan Roth
Elisha S. Rusch
Publication date: 01-09-2017
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 7/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1384-4

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Synaptic connections formed by patchy projections of pyramidal cells in the superficial layers of cat visual cortex

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