Skip to main content
Top
Published in: Brain Structure and Function 3/2020

01-04-2020 | Original Article

GABAergic and non-GABAergic subpopulations of Kv3.1b-expressing neurons in macaque V2 and MT: laminar distributions and proportion of total neuronal population

Authors: Jenna G. Kelly, Michael J. Hawken

Published in: Brain Structure and Function | Issue 3/2020

Login to get access

Abstract

The Kv3.1b potassium channel subunit, which facilitates the fast-spiking phenotype characteristic of parvalbumin (PV)-expressing inhibitory interneurons, is also expressed by subpopulations of excitatory neurons in macaque cortex. We have previously shown that V1 neurons expressing Kv3.1b but not PV or GABA were largely concentrated within layers 4Cα and 4B of V1, suggesting laminar or pathway specificity. In the current study, the distribution and pattern of co-immunoreactivity of GABA, PV, and Kv3.1b across layers in extrastriate cortical areas V2 and MT of the macaque monkey were measured using the same triple immunofluorescence labeling, confocal microscopy, and partially automated cell-counting strategies used in V1. For comparison, densities of the overall cell and neuronal populations were also measured for each layer of V2 and MT using tissue sections immunofluorescence labeled for the pan-neuronal marker NeuN. GABAergic neurons accounted for 14% of the total neuronal population in V2 and 25% in MT. Neurons expressing Kv3.1b but neither GABA nor PV were present in both areas. This subpopulation was most prevalent in the lowest subcompartment of layer 3, comprising 5% of the total neuronal population in layer 3C of both areas, and 41% and 36% of all Kv3.1b+ neurons in this layer in V2 and MT, respectively. The prevalence and laminar distribution of this subpopulation were remarkably consistent between V2 and MT and showed a striking similarity to the patterns observed previously in V1, suggesting a common contribution to the cortical circuit across areas.
Appendix
Available only for authorised users
Literature
go back to reference Balaram P, Kaas JH (2014) Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity. Front Neuroanat 8:81PubMedPubMedCentral Balaram P, Kaas JH (2014) Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity. Front Neuroanat 8:81PubMedPubMedCentral
go back to reference Balaram P, Young NA, Kaas JH (2014) Histological features of layers and sublayers in cortical visual areas V1 and V2 of chimpanzees, macaque monkeys, and humans. Eye Brain 6:5–18PubMedCentral Balaram P, Young NA, Kaas JH (2014) Histological features of layers and sublayers in cortical visual areas V1 and V2 of chimpanzees, macaque monkeys, and humans. Eye Brain 6:5–18PubMedCentral
go back to reference Beaulieu C, Kisvarday Z, Somogyi P, Cynader M, Cowey A (1992) Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb Cortex 2:295–309PubMed Beaulieu C, Kisvarday Z, Somogyi P, Cynader M, Cowey A (1992) Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb Cortex 2:295–309PubMed
go back to reference Brodmann K (1909) Localisation in the cerebral cortex. (Garey LJ, trans) Smith-Gordon, London Brodmann K (1909) Localisation in the cerebral cortex. (Garey LJ, trans) Smith-Gordon, London
go back to reference Casagrande VA, Kaas JH (1994) The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In: Peters A, Rockland K (eds) Cerebral cortex, vol. 10: primary visual cortex of primates. Plenum Press, New York, pp 201–259 Casagrande VA, Kaas JH (1994) The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In: Peters A, Rockland K (eds) Cerebral cortex, vol. 10: primary visual cortex of primates. Plenum Press, New York, pp 201–259
go back to reference Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894–3906PubMedPubMedCentral Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894–3906PubMedPubMedCentral
go back to reference Chow A, Erisir A, Nadal MS, Ozaita A, Lau D, Welker E, Rudy B (1999) K+ channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J Neurosci 19:9332–9345PubMedPubMedCentral Chow A, Erisir A, Nadal MS, Ozaita A, Lau D, Welker E, Rudy B (1999) K+ channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J Neurosci 19:9332–9345PubMedPubMedCentral
go back to reference Collins CE (2011) Variability in neuron densities across the cortical sheet in primates. Brain Behav Evol 78:37–50PubMed Collins CE (2011) Variability in neuron densities across the cortical sheet in primates. Brain Behav Evol 78:37–50PubMed
go back to reference Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH (2010) Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci 107:15927–15932PubMed Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH (2010) Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci 107:15927–15932PubMed
go back to reference Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994) Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95–116PubMed Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994) Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95–116PubMed
go back to reference Constantinople CM, Disney AA, Maffie J, Rudy B, Hawken MJ (2009) Quantitative analysis of neurons with Kv3 potassium channel subunits, Kv3.1b and Kv3.2, in macaque primary visual cortex. J Comp Neurol 516:291–311PubMedPubMedCentral Constantinople CM, Disney AA, Maffie J, Rudy B, Hawken MJ (2009) Quantitative analysis of neurons with Kv3 potassium channel subunits, Kv3.1b and Kv3.2, in macaque primary visual cortex. J Comp Neurol 516:291–311PubMedPubMedCentral
go back to reference Coppola JJ, Disney AA (2018) Most calbindin-immunoreactive neurons, but few calretinin-immunoreactive neurons, express the m1 acetylcholine receptor in the middle temporal visual area of the macaque monkey. Brain Behav 8:e01071PubMedPubMedCentral Coppola JJ, Disney AA (2018) Most calbindin-immunoreactive neurons, but few calretinin-immunoreactive neurons, express the m1 acetylcholine receptor in the middle temporal visual area of the macaque monkey. Brain Behav 8:e01071PubMedPubMedCentral
go back to reference DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299–316PubMed DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299–316PubMed
go back to reference DeFelipe J, González-Albo MC, Del Río MR, Elston GN (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412:515–526PubMed DeFelipe J, González-Albo MC, Del Río MR, Elston GN (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412:515–526PubMed
go back to reference Desimone R, Ungerleider LG (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248:164–189PubMed Desimone R, Ungerleider LG (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248:164–189PubMed
go back to reference Dhar P, Mehra RD, Sidharthan V, Sharma K (2001) Parvalbumin and calbindin D-28K immunoreactive neurons in area MT of rhesus monkey. Exp Brain Res 137:141–149PubMed Dhar P, Mehra RD, Sidharthan V, Sharma K (2001) Parvalbumin and calbindin D-28K immunoreactive neurons in area MT of rhesus monkey. Exp Brain Res 137:141–149PubMed
go back to reference Disney AA, Aoki C (2008) Muscarinic acetylcholine receptors in macaque V1 are most frequently expressed by parvalbumin-immunoreactive neurons. J Comp Neurol 507:1748–1762PubMedPubMedCentral Disney AA, Aoki C (2008) Muscarinic acetylcholine receptors in macaque V1 are most frequently expressed by parvalbumin-immunoreactive neurons. J Comp Neurol 507:1748–1762PubMedPubMedCentral
go back to reference Disney AA, Reynolds JH (2014) Expression of m1-type muscarinic acetylcholine receptors by parvalbumin-immunoreactive neurons in the primary visual cortex: a comparative study of rat, guinea pig, ferret, macaque, and human. J Comp Neurol 522:986–1003PubMedPubMedCentral Disney AA, Reynolds JH (2014) Expression of m1-type muscarinic acetylcholine receptors by parvalbumin-immunoreactive neurons in the primary visual cortex: a comparative study of rat, guinea pig, ferret, macaque, and human. J Comp Neurol 522:986–1003PubMedPubMedCentral
go back to reference Du J, Zhang L, Weiser M, Rudy B, McBain CJ (1996) Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J Neurosci 16:506–518PubMedPubMedCentral Du J, Zhang L, Weiser M, Rudy B, McBain CJ (1996) Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J Neurosci 16:506–518PubMedPubMedCentral
go back to reference Elston GN, Rosa MGP (1997) The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432–452PubMed Elston GN, Rosa MGP (1997) The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432–452PubMed
go back to reference Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K+ channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476–2489PubMed Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K+ channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476–2489PubMed
go back to reference Federer F, Ichida JM, Jeffs J, Schiessl I, McLoughlin N, Angelucci A (2009) Four projection streams from primate V1 to the cytochrome oxidase stripes of V2. J Neurosci 29:15455–15471PubMedPubMedCentral Federer F, Ichida JM, Jeffs J, Schiessl I, McLoughlin N, Angelucci A (2009) Four projection streams from primate V1 to the cytochrome oxidase stripes of V2. J Neurosci 29:15455–15471PubMedPubMedCentral
go back to reference Fries W, Distel H (1983) Large layer VI neurons of monkey striate cortex (Meynert cells) project to the superior colliculus. Proc R Soc Lond B 219:53–59PubMed Fries W, Distel H (1983) Large layer VI neurons of monkey striate cortex (Meynert cells) project to the superior colliculus. Proc R Soc Lond B 219:53–59PubMed
go back to reference Fries W, Keizer K, Kuypers HG (1985) Large layer VI cells in macaque striate cortex (Meynert cells) project to both superior colliculus and prestriate visual area V5. Exp Brain Res 58:613–616PubMed Fries W, Keizer K, Kuypers HG (1985) Large layer VI cells in macaque striate cortex (Meynert cells) project to both superior colliculus and prestriate visual area V5. Exp Brain Res 58:613–616PubMed
go back to reference Gabbott PL, Bacon SJ (1996) Local circuit neurons in the medial prefrontal cortex (areas 24a, b, c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J Comp Neurol 364:609–636PubMed Gabbott PL, Bacon SJ (1996) Local circuit neurons in the medial prefrontal cortex (areas 24a, b, c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J Comp Neurol 364:609–636PubMed
go back to reference García-Marín V, Ahmed TH, Afzal YC, Hawken MJ (2013) Distribution of the vesicular glutamate transporter 2 (vGluT2) in the primary visual cortex of the macaque and human. J Comp Neurol 521:130–151PubMedPubMedCentral García-Marín V, Ahmed TH, Afzal YC, Hawken MJ (2013) Distribution of the vesicular glutamate transporter 2 (vGluT2) in the primary visual cortex of the macaque and human. J Comp Neurol 521:130–151PubMedPubMedCentral
go back to reference Giannaris EL, Rosene DL (2012) A stereological study of the numbers of neurons and glia in the primary visual cortex across the lifespan of male and female rhesus monkeys. J Comp Neurol 520:3492–3508PubMedPubMedCentral Giannaris EL, Rosene DL (2012) A stereological study of the numbers of neurons and glia in the primary visual cortex across the lifespan of male and female rhesus monkeys. J Comp Neurol 520:3492–3508PubMedPubMedCentral
go back to reference Gittins R, Harrison PJ (2004) Neuronal density, size and shape in the human anterior cingulate cortex: a comparison of Nissl and NeuN staining. Brain Res Bull 63:155–160PubMed Gittins R, Harrison PJ (2004) Neuronal density, size and shape in the human anterior cingulate cortex: a comparison of Nissl and NeuN staining. Brain Res Bull 63:155–160PubMed
go back to reference Glickstein M, Whitteridge D (1976) Degeneration of layer III pyramidal cells in area 18 following destruction of callosal input. Brain Res 104:148–151PubMed Glickstein M, Whitteridge D (1976) Degeneration of layer III pyramidal cells in area 18 following destruction of callosal input. Brain Res 104:148–151PubMed
go back to reference Goris RLT, Simoncelli EP, Movshon JA (2015) Origin and function of tuning diversity in macaque visual cortex. Neuron 88:819–831PubMedPubMedCentral Goris RLT, Simoncelli EP, Movshon JA (2015) Origin and function of tuning diversity in macaque visual cortex. Neuron 88:819–831PubMedPubMedCentral
go back to reference Härtig W, Derouiche A, Welt K, Brauer K, Grosche J, Mäder M, Reichenbach A, Brückner G (1999) Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842:15–29PubMed Härtig W, Derouiche A, Welt K, Brauer K, Grosche J, Mäder M, Reichenbach A, Brückner G (1999) Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842:15–29PubMed
go back to reference Hӓssler R (1966) Comparative anatomy of the central visual systems in day and night-active primates. In: Hӓssler R, Stephan H (eds) Evolution of the forebrain. Thieme Verlag, Stuttgart, pp 419–434 Hӓssler R (1966) Comparative anatomy of the central visual systems in day and night-active primates. In: Hӓssler R, Stephan H (eds) Evolution of the forebrain. Thieme Verlag, Stuttgart, pp 419–434
go back to reference Hendrickson AE, Wilson JR, Ogren MP (1978) The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. J Comp Neurol 182:123–136PubMed Hendrickson AE, Wilson JR, Ogren MP (1978) The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. J Comp Neurol 182:123–136PubMed
go back to reference Hendry SHC, Jones EG, Emson PC, Lawson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467–472PubMed Hendry SHC, Jones EG, Emson PC, Lawson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467–472PubMed
go back to reference Hendry SHC, Schwark HD, Jones EG, Yan J (1987) Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503–1519PubMedPubMedCentral Hendry SHC, Schwark HD, Jones EG, Yan J (1987) Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503–1519PubMedPubMedCentral
go back to reference Hernández-Pineda R, Chow A, Amarillo Y, Moreno H, Saganich M, Vega-Saenz de Miera E, Hernández-Cruz A, Rudy B (1999) Kv3.1–Kv3.2 channels underlie a high-voltage-activating component of the delayed rectifier K+ current in projecting neurons from the globus pallidus. J Neurophysiol 82:1512–1528PubMed Hernández-Pineda R, Chow A, Amarillo Y, Moreno H, Saganich M, Vega-Saenz de Miera E, Hernández-Cruz A, Rudy B (1999) Kv3.1–Kv3.2 channels underlie a high-voltage-activating component of the delayed rectifier K+ current in projecting neurons from the globus pallidus. J Neurophysiol 82:1512–1528PubMed
go back to reference Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161–186PubMed Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161–186PubMed
go back to reference Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec A Discov Mol Cell Evol Biol 287A:1153–1163 Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec A Discov Mol Cell Evol Biol 287A:1153–1163
go back to reference Hof PR, Ungerleider LG, Webster MJ, Gattass R, Adams MM, Sailstad CA, Morrison JH (1996) Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. J Comp Neurol 376:112–127PubMed Hof PR, Ungerleider LG, Webster MJ, Gattass R, Adams MM, Sailstad CA, Morrison JH (1996) Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. J Comp Neurol 376:112–127PubMed
go back to reference Horton JC (1984) Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philos Trans R Soc Lond B 304:199–253 Horton JC (1984) Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philos Trans R Soc Lond B 304:199–253
go back to reference Howard V, Reid S, Baddeley A, Boyde A (1985) Unbiased estimation of particle density in the tandem scanning reflected light microscope. J Microsc 138:203–212PubMed Howard V, Reid S, Baddeley A, Boyde A (1985) Unbiased estimation of particle density in the tandem scanning reflected light microscope. J Microsc 138:203–212PubMed
go back to reference Hubel DH, Wiesel TN (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol 146:421–450PubMed Hubel DH, Wiesel TN (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol 146:421–450PubMed
go back to reference Ichinohe N, Watakabe A, Miyashita T, Yamamori T, Hashikawa T, Rockland KS (2004) A voltage-gated potassium channel, Kv3.1b, is expressed by a subpopulation of large pyramidal neurons in layer 5 of the macaque monkey cortex. Neuroscience 129:179–185PubMed Ichinohe N, Watakabe A, Miyashita T, Yamamori T, Hashikawa T, Rockland KS (2004) A voltage-gated potassium channel, Kv3.1b, is expressed by a subpopulation of large pyramidal neurons in layer 5 of the macaque monkey cortex. Neuroscience 129:179–185PubMed
go back to reference Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387–396PubMed Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387–396PubMed
go back to reference Kawaguchi Y, Kubota Y (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neurosci 85:677–701 Kawaguchi Y, Kubota Y (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neurosci 85:677–701
go back to reference Kelly JG, García-Marín V, Rudy B, Hawken MJ (2019) Densities and laminar distributions of Kv3.1b-, PV-, GABA-, and SMI-32-immunoreactive neurons in macaque area V1. Cereb Cortex 29:1921–1937PubMed Kelly JG, García-Marín V, Rudy B, Hawken MJ (2019) Densities and laminar distributions of Kv3.1b-, PV-, GABA-, and SMI-32-immunoreactive neurons in macaque area V1. Cereb Cortex 29:1921–1937PubMed
go back to reference Kelly JG, Hawken MJ (2017) Quantification of neuronal density across cortical depth using automated 3D analysis of confocal image stacks. Brain Struct Funct 222:3333–3353PubMedPubMedCentral Kelly JG, Hawken MJ (2017) Quantification of neuronal density across cortical depth using automated 3D analysis of confocal image stacks. Brain Struct Funct 222:3333–3353PubMedPubMedCentral
go back to reference Kennedy H, Dehay C, Bullier J (1986) Organization of the callosal connections of visual areas V1 and V2 in the macaque monkey. J Comp Neurol 247:398–415PubMed Kennedy H, Dehay C, Bullier J (1986) Organization of the callosal connections of visual areas V1 and V2 in the macaque monkey. J Comp Neurol 247:398–415PubMed
go back to reference Kondo H, Hashikawa T, Tanaka K, Jones EG (1994) Neurochemical gradient along the monkey occipito-temporal cortical pathway. NeuroReport 5:613–616PubMed Kondo H, Hashikawa T, Tanaka K, Jones EG (1994) Neurochemical gradient along the monkey occipito-temporal cortical pathway. NeuroReport 5:613–616PubMed
go back to reference Livingstone MS, Hubel DH (1987) Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey. J Neurosci 7:3371–3377PubMedPubMedCentral Livingstone MS, Hubel DH (1987) Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey. J Neurosci 7:3371–3377PubMedPubMedCentral
go back to reference Lund JS (1973) Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). J Comp Neurol 147:455–496PubMed Lund JS (1973) Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). J Comp Neurol 147:455–496PubMed
go back to reference Lund JS, Hendrickson AE, Ogren MP, Tobin EA (1981) Anatomical organization of primate visual cortex area VII. J Comp Neurol 202:19–45PubMed Lund JS, Hendrickson AE, Ogren MP, Tobin EA (1981) Anatomical organization of primate visual cortex area VII. J Comp Neurol 202:19–45PubMed
go back to reference Lund JS, Lund RD, Hendrickson AE, Bunt AH, Fuchs AF (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164:287–304PubMed Lund JS, Lund RD, Hendrickson AE, Bunt AH, Fuchs AF (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164:287–304PubMed
go back to reference Maunsell JH, Van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3:2563–2586PubMedPubMedCentral Maunsell JH, Van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3:2563–2586PubMedPubMedCentral
go back to reference Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379:113–132PubMed Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379:113–132PubMed
go back to reference Meyer HS, Schwarz D, Wimmer VC, Schmitt AC, Kerr JND, Sakmann B, Helmstaedter M (2011) Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc Natl Acad Sci 108:16807–16812PubMed Meyer HS, Schwarz D, Wimmer VC, Schmitt AC, Kerr JND, Sakmann B, Helmstaedter M (2011) Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc Natl Acad Sci 108:16807–16812PubMed
go back to reference Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–211PubMed Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–211PubMed
go back to reference Nhan HL, Callaway EM (2012) Morphology of superior-colliculus- and middle temporal area-projecting neurons in primate primary visual cortex. J Comp Neurol 520:52–80PubMed Nhan HL, Callaway EM (2012) Morphology of superior-colliculus- and middle temporal area-projecting neurons in primate primary visual cortex. J Comp Neurol 520:52–80PubMed
go back to reference Pistorio AL, Hendry SH, Wang X (2006) A modified technique for high-resolution staining of myelin. J Neurosci Methods 153:135–146PubMed Pistorio AL, Hendry SH, Wang X (2006) A modified technique for high-resolution staining of myelin. J Neurosci Methods 153:135–146PubMed
go back to reference Povysheva NV, Zaitsev AV, Kröner S, Krimer OA, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS (2007) Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J Neurophysiol 97:1030–1039PubMed Povysheva NV, Zaitsev AV, Kröner S, Krimer OA, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS (2007) Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J Neurophysiol 97:1030–1039PubMed
go back to reference Povysheva NV, Zaitsev AV, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS (2008) Parvalbumin-positive basket interneurons in monkey and rat prefrontal cortex. J Neurophysiol 100:2348–2360PubMedPubMedCentral Povysheva NV, Zaitsev AV, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS (2008) Parvalbumin-positive basket interneurons in monkey and rat prefrontal cortex. J Neurophysiol 100:2348–2360PubMedPubMedCentral
go back to reference Preuss TM (2001) The discovery of cerebral diversity: an unwelcome scientific revolution. In: Falk D, Gibson KR (eds) Evolutionary anatomy of the primate cerebral cortex. Cambridge University Press, Cambridge, pp 138–164 Preuss TM (2001) The discovery of cerebral diversity: an unwelcome scientific revolution. In: Falk D, Gibson KR (eds) Evolutionary anatomy of the primate cerebral cortex. Cambridge University Press, Cambridge, pp 138–164
go back to reference Renier N, Wu Z, Simon DJ, Yang J, Ariel P, Tessier-Lavigne M (2014) iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159:896–910PubMed Renier N, Wu Z, Simon DJ, Yang J, Ariel P, Tessier-Lavigne M (2014) iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159:896–910PubMed
go back to reference Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in structure of the neocortex. Brain 103:221–244PubMed Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in structure of the neocortex. Brain 103:221–244PubMed
go back to reference Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:3–20PubMed Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:3–20PubMed
go back to reference Rudy B, Chow A, Lau D, Amarillo Y, Ozaita A, Saganich M, Moreno H, Nadal MS, Hernández-Pineda R, Hernández-Cruz A, Erisir A, Leonard C, Vega-Saenz de Miera E (1999) Contributions of Kv3 channels to neuronal excitability. Ann N Y Acad Sci 868:304–343PubMed Rudy B, Chow A, Lau D, Amarillo Y, Ozaita A, Saganich M, Moreno H, Nadal MS, Hernández-Pineda R, Hernández-Cruz A, Erisir A, Leonard C, Vega-Saenz de Miera E (1999) Contributions of Kv3 channels to neuronal excitability. Ann N Y Acad Sci 868:304–343PubMed
go back to reference Saleem KS, Logothetis NK (2007) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxis coordinates. Academic Press, London Saleem KS, Logothetis NK (2007) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxis coordinates. Academic Press, London
go back to reference Sherwood CC, Raghanti MA, Stimpson CD, Bonar CJ, deSousa AA, Preuss TM, Hof PR (2007) Scaling of inhibitory interneurons in areas V1 and V2 of anthropoid primates as revealed by calcium binding protein immunohistochemistry. Brain Behav Evol 69:176–195PubMed Sherwood CC, Raghanti MA, Stimpson CD, Bonar CJ, deSousa AA, Preuss TM, Hof PR (2007) Scaling of inhibitory interneurons in areas V1 and V2 of anthropoid primates as revealed by calcium binding protein immunohistochemistry. Brain Behav Evol 69:176–195PubMed
go back to reference Shi SR, Key ME, Kalra KL (1991) Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J Histochem Cytochem 39:741–748PubMed Shi SR, Key ME, Kalra KL (1991) Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J Histochem Cytochem 39:741–748PubMed
go back to reference Shipp S, Zeki S (1985) Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315:322–324PubMed Shipp S, Zeki S (1985) Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315:322–324PubMed
go back to reference Shipp S, Zeki S (1989) The organization of connections between areas V5 and V2 in macaque monkey visual cortex. Eur J Neurosci 1:333–354PubMed Shipp S, Zeki S (1989) The organization of connections between areas V5 and V2 in macaque monkey visual cortex. Eur J Neurosci 1:333–354PubMed
go back to reference Shipp S, Zeki S (1995) Segregation and convergence of specialized pathways in macaque monkey visual cortex. J Anat 187:547–562PubMedPubMedCentral Shipp S, Zeki S (1995) Segregation and convergence of specialized pathways in macaque monkey visual cortex. J Anat 187:547–562PubMedPubMedCentral
go back to reference Soares D, Goldrick I, Lemon RN, Kraskov A, Greensmith L, Kalmar B (2017) Expression of Kv3.1b potassium channel is widespread in macaque motor cortex pyramidal cells: a histological comparison between rat and macaque. J Comp Neurol 525:2164–2174PubMedPubMedCentral Soares D, Goldrick I, Lemon RN, Kraskov A, Greensmith L, Kalmar B (2017) Expression of Kv3.1b potassium channel is widespread in macaque motor cortex pyramidal cells: a histological comparison between rat and macaque. J Comp Neurol 525:2164–2174PubMedPubMedCentral
go back to reference Spatz WB, Tigges J, Tigges M (1970) Subcortical projections, cortical associations, and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey (Saimiri). J Comp Neurol 140:155–174PubMed Spatz WB, Tigges J, Tigges M (1970) Subcortical projections, cortical associations, and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey (Saimiri). J Comp Neurol 140:155–174PubMed
go back to reference Srinivasan S, Carlo CN, Stevens CF (2015) Predicting visual acuity from the structure of visual cortex. Proc Natl Acad Sci 112:7815–7820PubMed Srinivasan S, Carlo CN, Stevens CF (2015) Predicting visual acuity from the structure of visual cortex. Proc Natl Acad Sci 112:7815–7820PubMed
go back to reference Tootell RB, Taylor JB (1995) Anatomical evidence for MT and additional cortical visual areas in humans. Cereb Cortex 5:39–55PubMed Tootell RB, Taylor JB (1995) Anatomical evidence for MT and additional cortical visual areas in humans. Cereb Cortex 5:39–55PubMed
go back to reference Turner EC, Young NA, Reed JL, Collins CE, Flaherty DK, Gabi M, Kaas JH (2016) Distribution of cells and neurons across the cortical sheet in Old World macaques. Brain Behav Evol 88:1–13PubMed Turner EC, Young NA, Reed JL, Collins CE, Flaherty DK, Gabi M, Kaas JH (2016) Distribution of cells and neurons across the cortical sheet in Old World macaques. Brain Behav Evol 88:1–13PubMed
go back to reference Valverde F (1978) The organization of area 18 in the monkey. Anat Embryol 154:305–334PubMed Valverde F (1978) The organization of area 18 in the monkey. Anat Embryol 154:305–334PubMed
go back to reference van Brederode JFM, Mulligan KA, Hendrickson AE (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298:1–22PubMed van Brederode JFM, Mulligan KA, Hendrickson AE (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298:1–22PubMed
go back to reference Vickers JC, Huntley GW, Edwards AM, Moran T, Rogers SW, Heinemann SF, Morrison JH (1993) Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. J Neurosci 13:2962–2992 Vickers JC, Huntley GW, Edwards AM, Moran T, Rogers SW, Heinemann SF, Morrison JH (1993) Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. J Neurosci 13:2962–2992
go back to reference Vigneswaran G, Kraskov A, Lemon RN (2011) Large identified pyramidal cells in macaque motor and premotor cortex exhibit “thin spikes”: implications for cell type classification. J Neurosci 31:14235–14242PubMedPubMedCentral Vigneswaran G, Kraskov A, Lemon RN (2011) Large identified pyramidal cells in macaque motor and premotor cortex exhibit “thin spikes”: implications for cell type classification. J Neurosci 31:14235–14242PubMedPubMedCentral
go back to reference von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana
go back to reference von Economo C (1927) Zellaufbau der Grosshirnrinde des Menschen. Verlag Julius Springer, Berlin. English edition: von Economo C (1927) Cellular structure of the human cerebral cortex (trans: Triarhou LC). Karger, Basel von Economo C (1927) Zellaufbau der Grosshirnrinde des Menschen. Verlag Julius Springer, Berlin. English edition: von Economo C (1927) Cellular structure of the human cerebral cortex (trans: Triarhou LC). Karger, Basel
go back to reference Wang L-Y, Gan L, Forsythe ID, Kaczmarek LK (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J Physiol 509:183–194PubMedPubMedCentral Wang L-Y, Gan L, Forsythe ID, Kaczmarek LK (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J Physiol 509:183–194PubMedPubMedCentral
go back to reference Weiser M, Bueno E, Sekirnjak C, Martone ME, Baker H, Hillman D, Chen S, Thornhill W, Ellisman M, Rudy B (1995) The potassium channel subunit Kv3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J Neurosci 15:4298–4314PubMedPubMedCentral Weiser M, Bueno E, Sekirnjak C, Martone ME, Baker H, Hillman D, Chen S, Thornhill W, Ellisman M, Rudy B (1995) The potassium channel subunit Kv3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J Neurosci 15:4298–4314PubMedPubMedCentral
go back to reference Williams RW, Rakic P (1988) Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J Comp Neurol 278:344–352PubMed Williams RW, Rakic P (1988) Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J Comp Neurol 278:344–352PubMed
go back to reference Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blümcke I (1996) NeuN: a useful marker for diagnostic histopathology. J Histochem Cytochem 44:1167–1171PubMed Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blümcke I (1996) NeuN: a useful marker for diagnostic histopathology. J Histochem Cytochem 44:1167–1171PubMed
go back to reference Wong-Riley MTT (1974) Demonstration of geniculocortical and callosal projection neurons in the squirrel monkey by means of retrograde axonal transport of horseradish peroxidase. Brain Res 79:267–272PubMed Wong-Riley MTT (1974) Demonstration of geniculocortical and callosal projection neurons in the squirrel monkey by means of retrograde axonal transport of horseradish peroxidase. Brain Res 79:267–272PubMed
go back to reference Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28PubMed Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28PubMed
go back to reference Yoshioka T, Levitt JB, Lund JS (1994) Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: anatomy of interlaminar projections. Vis Neurosci 11:467–489PubMed Yoshioka T, Levitt JB, Lund JS (1994) Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: anatomy of interlaminar projections. Vis Neurosci 11:467–489PubMed
go back to reference Zeki S, Shipp S (1989) Modular connections between areas V2 and V4 of macaque monkey visual cortex. Eur J Neurosci 1:494–506PubMed Zeki S, Shipp S (1989) Modular connections between areas V2 and V4 of macaque monkey visual cortex. Eur J Neurosci 1:494–506PubMed
go back to reference Zeng H, Shen EH, Hohmann JG, Oh SW, Bernard A, Royall JJ, Glattfelder KJ, Sunkin SM, Morris JA, Guillozet-Bongaarts AL, Smith KA, Ebbert AJ, Swanson B, Kuan L, Page DT, Overly CC, Lein ES, Hawrylycz MJ, Hof PR, Hyde TM, Kleinman JE, Jones AR (2012) Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 149:483–496PubMedPubMedCentral Zeng H, Shen EH, Hohmann JG, Oh SW, Bernard A, Royall JJ, Glattfelder KJ, Sunkin SM, Morris JA, Guillozet-Bongaarts AL, Smith KA, Ebbert AJ, Swanson B, Kuan L, Page DT, Overly CC, Lein ES, Hawrylycz MJ, Hof PR, Hyde TM, Kleinman JE, Jones AR (2012) Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 149:483–496PubMedPubMedCentral
go back to reference Ziemba CM, Freeman J, Simoncelli EP, Movshon JA (2018) Contextual modulation of sensitivity to naturalistic image structure in macaque V2. J Neurophysiol 120:409–420PubMedPubMedCentral Ziemba CM, Freeman J, Simoncelli EP, Movshon JA (2018) Contextual modulation of sensitivity to naturalistic image structure in macaque V2. J Neurophysiol 120:409–420PubMedPubMedCentral
go back to reference Ziemba CM, Perez RK, Pai J, Kelly JG, Hallum LE, Shooner C, Movshon JA (2019) Laminar differences in responses to naturalistic texture in macaque V1 and V2. J Neurosci 39:9748–9756PubMed Ziemba CM, Perez RK, Pai J, Kelly JG, Hallum LE, Shooner C, Movshon JA (2019) Laminar differences in responses to naturalistic texture in macaque V1 and V2. J Neurosci 39:9748–9756PubMed
Metadata
Title
GABAergic and non-GABAergic subpopulations of Kv3.1b-expressing neurons in macaque V2 and MT: laminar distributions and proportion of total neuronal population
Authors
Jenna G. Kelly
Michael J. Hawken
Publication date
01-04-2020
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02065-y

Other articles of this Issue 3/2020

Brain Structure and Function 3/2020 Go to the issue