Top

Published in:

Open Access 01-05-2018 | Original Article

Translaminar circuits formed by the pyramidal cells in the superficial layers of cat visual cortex

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

Published in: Brain Structure and Function | Issue 4/2018

Abstract

Pyramidal cells in the superficial layers of the neocortex provide a major excitatory projection to layer 5, which contains the pyramidal cells that project to subcortical motor-related targets. Both structurally and functionally rather little is known about this interlaminar pathway, especially in higher mammals. Here, we made sparse ultrastructural reconstructions of the projection to layer 5 of three pyramidal neurons from layer 3 in cat V1 whose morphology, physiology, and synaptic connections with layers 2 and 3 were known. The dominant targets of the 74 identified synapses in layer 5 were the dendritic spines of pyramidal cells. The fractions of target spiny dendrites were 59, 61, and 84% for the three cells, with the remaining targets being dendrites of smooth neurons. These fractions were similar to the distribution of targets of unlabeled asymmetric synapses in the surrounding neuropil. Serial section reconstructions revealed that the target dendrites were heterogenous in morphology, indicating that different cell types are innervated. This new evidence indicates that the descending projection from the superficial layer pyramidal cells does not simply drive the output pyramidal cells that project to cortical and subcortical targets, but participates in the complex circuitry of the deep cortical layers.

Ahmed B, Anderson JC, Martin KA, Nelson JC (1997) Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J Comp Neurol 380(2):230–242PubMedCrossRef

Anderson JC, Martin KA (2001) Does bouton morphology optimize axon length? Nat Neurosci 4(12):1166–1167. https://doi.org/10.1038/nn772 PubMedCrossRef

Anderson JC, Douglas RJ, Martin KA, Nelson JC (1994) Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J Comp Neurol 341(1):25–38. https://doi.org/10.1002/cne.903410104 PubMedCrossRef

Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84(2):909–926PubMedCrossRef

Anderson JC, da Costa NM, Martin KA (2009) The W cell pathway to cat primary visual cortex. J Comp Neurol 516(1):20–35. https://doi.org/10.1002/cne.22085 PubMedCrossRef

Bartol TM, Bromer C, Kinney J, Chirillo MA, Bourne JN, Harris KM, Sejnowski TJ (2015) Nanoconnectomic upper bound on the variability of synaptic plasticity. eLife 4:e10778. https://doi.org/10.7554/eLife.10778 PubMedPubMedCentralCrossRef

Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76(4):695–711. https://doi.org/10.1016/j.neuron.2012.10.038 PubMedPubMedCentralCrossRef

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

Binzegger T, Douglas RJ, Martin KA (2007) Stereotypical bouton clustering of individual neurons in cat primary visual cortex. J Neurosci 27(45):12242–12254. https://doi.org/10.1523/JNEUROSCI.3753-07.2007 PubMedCrossRef

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, pp 55–97

Bopp R, Maçarico 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. https://doi.org/10.1371/journal.pbio.1001932 PubMedPubMedCentralCrossRef

Borg-Graham LJ, Monier C, Fregnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393(6683):369–373. https://doi.org/10.1038/30735 PubMedCrossRef

Braitenberg V, Schüz A (1991) Peters’ rule and white’s exception. Springer, Berlin, pp 109–112

Braitenberg V, Schüz A (2013) Cortex: statistics and geometry of neuronal connectivity. Springer, Berlin

Briggman KL, Bock DD (2012) Volume electron microscopy for neuronal circuit reconstruction. Curr Opin Neurobiol 22(1):154–161. https://doi.org/10.1016/j.conb.2011.10.022 PubMedCrossRef

Bullier J, Kennedy H, Salinger W (1984) Branching and laminar origin of projections between visual cortical areas in the cat. J Comp Neurol 228(3):329–341. https://doi.org/10.1002/cne.902280304 PubMedCrossRef

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. https://doi.org/10.1371/journal.pone.0038011 PubMedPubMedCentralCrossRef

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

Cunningham ET Jr, Levay S (1986) Laminar and synaptic organization of the projection from the thalamic nucleus centralis to primary visual cortex in the cat. J Comp Neurol 254(1):66–77PubMedCrossRef

D - NLM: PMC2602799 EDAT- 2008/09/06 09:00 MHDA- 2009/02/10 09:00 CRDT- 2008/09/06 09:00 PHST- 2008/03/21 [received] PHST- 2008/08/11 [revised] PHST- 2008/08/11 [accepted] PHST- 2008/08/22 [aheadofprint] AID - S0006–8993(08)02034-9 [pii] AID – 10.1016/j.brainres.2008.08.029 [doi] PST - ppublish

DeFelipe J, Farinas I (1992) The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 39(6):563–607PubMedCrossRef

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

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

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

Douglas RJ, Martin KA, Whitteridge D (1991) An intracellular analysis of the visual responses of neurones in cat visual cortex. J Physiol 440:659–696PubMedPubMedCentralCrossRef

Einstein G (1996) Reciprocal projections of cat extrastriate cortex: I. Distribution and morphology of neurons projecting from posterior medial lateral suprasylvian sulcus to area 17. J Comp Neurol 376(4):518–529. https://doi.org/10.1002/(SICI)1096-9861(19961223)376:4<518::AID-CNE2>3.0.CO;2-4 PubMedCrossRef

Einstein G, Fitzpatrick D (1991) Distribution and morphology of area 17 neurons that project to the cat’s extrastriate cortex. J Comp Neurol 303(1):132–149. https://doi.org/10.1002/cne.903030112 PubMedCrossRef

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. https://doi.org/10.1523/jneurosci.0474-13.2014 PubMedCrossRef

Gabbott PL, Martin KA, Whitteridge D (1987) Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17). J Comp Neurol 259(3):364–381. https://doi.org/10.1002/cne.902590305 PubMedCrossRef

Gawne TJ, Kjaer TW, Hertz JA, Richmond BJ (1996) Adjacent visual cortical complex cells share about 20% of their stimulus-related information. Cereb Cortex 6(3):482–489PubMedCrossRef

Gilbert CD (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J Physiol 268(2):391–421PubMedPubMedCentralCrossRef

Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3(5):1116–1133PubMedCrossRef

Hirsch JA, Gallagher CA, Alonso JM, Martinez LM (1998) Ascending projections of simple and complex cells in layer 6 of the cat striate cortex. J Neurosci 18(19):8086–8094PubMedCrossRef

Hirsch JA, Martinez LM, Pillai C, Alonso JM, Wang Q, Sommer FT (2003) Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat Neurosci 6(12):1300–1308. https://doi.org/10.1038/nn1152 PubMedCrossRef

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

Hubener M, Schwarz C, Bolz J (1990) Morphological types of projection neurons in layer 5 of cat visual cortex. J Comp Neurol 301(4):655–674. https://doi.org/10.1002/cne.903010412 PubMedCrossRef

Katz LC (1987) Local circuitry of identified projection neurons in cat visual cortex brain slices. J Neurosci 7(4):1223–1249PubMedCrossRef

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. https://doi.org/10.1523/jneurosci.0906-15.2015 PubMedCrossRef

Kisvarday ZF, Martin KA, Whitteridge D, Somogyi P (1985) Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol 241(2):111–137. https://doi.org/10.1002/cne.902410202 PubMedCrossRef

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):541–552PubMedCrossRef

Kisvarday ZF, Martin KA, Friedlander MJ, Somogyi P (1987) Evidence for interlaminar inhibitory circuits in the striate cortex of the cat. J Comp Neurol 260(1):1–19. https://doi.org/10.1002/cne.902600102 PubMedCrossRef

Koestinger G, Martin KA, Roth S, Rusch ES (2017) Synaptic connections formed by patchy projections of pyramidal cells in the superficial layers of cat visual cortex. Brain Struct Funct. https://doi.org/10.1007/s00429-017-1384-4 PubMedCentral

Landau ID, Egger R, Dercksen VJ, Oberlaender M, Sompolinsky H (2016) The impact of structural heterogeneity on excitation-inhibition balance in cortical networks. Neuron 92(5):1106–1121. https://doi.org/10.1016/j.neuron.2016.10.027 PubMedPubMedCentralCrossRef

Lund JS, Henry GH, MacQueen CL, Harvey AR (1979) Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey. J Comp Neurol 184(4):599–618. https://doi.org/10.1002/cne.901840402 PubMedCrossRef

Markram H, Lubke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500(Pt 2):409–440PubMedPubMedCentralCrossRef

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

Martin KA, Schroder S (2016) Phase locking of multiple single neurons to the local field potential in cat V1. J Neurosci 36(8):2494–2502. https://doi.org/10.1523/jneurosci.2547-14.2016 PubMedCrossRef

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

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

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. https://doi.org/10.1038/ncomms6252 PubMedPubMedCentralCrossRef

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

Martin KA, Roth S, Rusch ES (2017) A biological blueprint for the axons of superficial layer pyramidal cells in cat primary visual cortex. Brain Struct Funct. https://doi.org/10.1007/s00429-017-1410-6

Martinez LM, Alonso JM, Reid RC, Hirsch JA (2002) Laminar processing of stimulus orientation in cat visual cortex. J Physiol 540(Pt 1):321–333PubMedPubMedCentralCrossRef

Meyer G (1983) Axonal patterns and topography of short-axon neurons in visual areas 17, 18, and 19 of the cat. J Comp Neurol 220(4):405–438. https://doi.org/10.1002/cne.902200405 PubMedCrossRef

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):663–680PubMedCrossRef

Nagerl UV, Kostinger G, Anderson JC, Martin KA, Bonhoeffer T (2007) Protracted synaptogenesis after activity-dependent spinogenesis in hippocampal neurons. J Neurosci 27(30):8149–8156. https://doi.org/10.1523/jneurosci.0511-07.2007 PubMedCrossRef

O’Leary JL (1941) Structure of the area striata of the cat. J Comp Neurol 75(1):131–164. https://doi.org/10.1002/cne.900750107 CrossRef

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):419–446PubMedPubMedCentralCrossRef

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

Reich DS, Mechler F, Victor JD (2001) Independent and redundant information in nearby cortical neurons. Science 294(5551):2566–2568. https://doi.org/10.1126/science.1065839 PubMedCrossRef

Schmid AM (2008) The processing of feature discontinuities for different cue types in primary visual cortex. Brain Res 1238:59–74. https://doi.org/10.1016/j.brainres.2008.08.029 PubMedPubMedCentralCrossRef

Schmidt KE (2013) The visual callosal connection: a connection like any other? Neural Plast. https://doi.org/10.1155/2013/397176 PubMedPubMedCentral

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

Silver RA, Lubke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302(5652):1981–1984. https://doi.org/10.1126/science.1087160 PubMedCrossRef

Somogyi P, Kisvarday ZF, Martin KA, Whitteridge D (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10(2):261–294PubMedCrossRef

Somogyi P, Freund TF, Hodgson AJ, Somogyi J, Beroukas D, Chubb IW (1985) Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res 332(1):143–149PubMedCrossRef

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

Thomson AM, West DC, Wang Y, Bannister AP (2002) Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2–5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12(9):936–953PubMedCrossRef

Weliky M, Fiser J, Hunt RH, Wagner DN (2003) Coding of natural scenes in primary visual cortex. Neuron 37(4):703–718PubMedCrossRef

Xu X, Olivas ND, Ikrar T, Peng T, Holmes TC, Nie Q, Shi Y (2016) Primary visual cortex shows laminar-specific and balanced circuit organization of excitatory and inhibitory synaptic connectivity. J Physiol 594(7):1891–1910. https://doi.org/10.1113/jp271891 PubMedPubMedCentralCrossRef

Yen SC, Baker J, Gray CM (2007) Heterogeneity in the responses of adjacent neurons to natural stimuli in cat striate cortex. J Neurophysiol 97(2):1326–1341. https://doi.org/10.1152/jn.00747.2006 PubMedCrossRef

Title: Translaminar circuits formed by the pyramidal cells in the superficial layers of cat visual cortex
Authors: German Koestinger
Kevan A. C. Martin
Elisha S. Rusch
Publication date: 01-05-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1588-7

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Translaminar circuits formed by the pyramidal cells in the superficial layers of cat visual cortex

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

GABAergic and non-GABAergic projections to the superior colliculus from the auditory brainstem

Neural circuits underlying jaw movements for the prey-catching behavior in frog: distribution of vestibular afferent terminals on motoneurons supplying the jaw

Diffusion tractography reveals pervasive asymmetry of cerebral white matter tracts in the bottlenose dolphin (Tursiops truncatus)

Sensory properties of the caudal aspect of the macaque’s superior parietal lobule

Receptor-driven, multimodal mapping of the human amygdala

Investigation of brain structure in the 1-month infant