1932

Abstract

Many of our daily activities, such as riding a bike to work or reading a book in a noisy cafe, and highly skilled activities, such as a professional playing a tennis match or a violin concerto, depend upon the ability of the brain to quickly make moment-to-moment adjustments to our behavior in response to the results of our actions. Particularly, they depend upon the ability of the neocortex to integrate the information provided by the sensory organs (bottom-up information) with internally generated signals such as expectations or attentional signals (top-down information). This integration occurs in pyramidal cells (PCs) and their long apical dendrite, which branches extensively into a dendritic tuft in layer 1 (L1). The outermost layer of the neocortex, L1 is highly conserved across cortical areas and species. Importantly, L1 is the predominant input layer for top-down information, relayed by a rich, dense mesh of long-range projections that provide signals to the tuft branches of the PCs. Here, we discuss recent progress in our understanding of the composition of L1 and review evidence that L1 processing contributes to functions such as sensory perception, cross-modal integration, controlling states of consciousness, attention, and learning.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-100520-012117
2021-07-08
2024-04-22
Loading full text...

Full text loading...

/deliver/fulltext/neuro/44/1/annurev-neuro-100520-012117.html?itemId=/content/journals/10.1146/annurev-neuro-100520-012117&mimeType=html&fmt=ahah

Literature Cited

  1. Abs E, Poorthuis RB, Apelblat D, Muhammad K, Pardi MB et al. 2018. Learning-related plasticity in dendrite-targeting layer 1 interneurons. Neuron 100:68499.e6
    [Google Scholar]
  2. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M 2012. A neural circuit for spatial summation in visual cortex. Nature 490:226–31
    [Google Scholar]
  3. Allaway KC, Muñoz W, Tremblay R, Sherer M, Herron J et al. 2020. Cellular birthdate predicts laminar and regional cholinergic projection topography in the forebrain. eLife 9:e63249
    [Google Scholar]
  4. Anastasiades PG, Collins DP, Carter AG 2020. Mediodorsal and ventromedial thalamus engage distinct L1 circuits in the prefrontal cortex. Neuron 109:314–30.e4
    [Google Scholar]
  5. Arezzo JC, Vaughan HG Jr, Legatt AD 1981. Topography and intracranial sources of somatosensory evoked potentials in the monkey. II. Cortical components. Electroencephalogr. Clin. Neurophysiol. 51:1–18
    [Google Scholar]
  6. Audet MA, Doucet G, Oleskevich S, Descarries L 1988. Quantified regional and laminar distribution of the noradrenaline innervation in the anterior half of the adult rat cerebral cortex. J. Comp. Neurol. 274:307–18
    [Google Scholar]
  7. Aveñdano C, Umbriaco D, Dykes RW, Descarries L 1996. Acetylcholine innervation of sensory and motor neocortical areas in adult cat: a choline acetyltransferase immunohistochemical study. J. Chem. Neuroanat. 11:113–30
    [Google Scholar]
  8. Awasthi JR, Tamada K, Overton ETN, Takumi T 2021. Comprehensive topographical map of the serotonergic fibers in the mouse brain. J. Comp. Neurol 529:1391429
    [Google Scholar]
  9. Barbas H, Pandya DN. 1989. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286:353–75
    [Google Scholar]
  10. Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ 2012. Canonical microcircuits for predictive coding. Neuron 76:695–711
    [Google Scholar]
  11. Bear MF, Carnes KM, Ebner FF 1985. An investigation of cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry. J. Comp. Neurol. 234:411–30
    [Google Scholar]
  12. Beierlein M, Gibson JR, Connors BW 2003. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90:2987–3000
    [Google Scholar]
  13. Benevento LA, Ebner FF. 1971. The areas and layers of corticocortical terminations in the visual cortex of the Virginia opossum. J. Comp. Neurol. 141:157–89
    [Google Scholar]
  14. Berger B, Tassin JP, Blanc G, Moyne MA, Thierry AM 1974. Histochemical confirmation for dopaminergic innervation of the rat cerebral cortex after destruction of the noradrenergic ascending pathways. Brain Res. 81:332–37
    [Google Scholar]
  15. Berger B, Trottier S, Verney C, Gaspar P, Alvarez C 1988. Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: a radioautographic study. J. Comp. Neurol. 273:99–119
    [Google Scholar]
  16. Björklund A, Divac I, Lindvall O 1978. Regional distribution of catecholamines in monkey cerebral cortex, evidence for a dopaminergic innervation of the primate prefrontal cortex. Neurosci. Lett. 7:115–19
    [Google Scholar]
  17. Boldog E, Bakken TE, Hodge RD, Novotny M, Aevermann BD et al. 2018. Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type. Nat. Neurosci. 21:1185–95
    [Google Scholar]
  18. Bolkan SS, Stujenske JM, Parnaudeau S, Spellman TJ, Rauffenbart C et al. 2017. Thalamic projections sustain prefrontal activity during working memory maintenance. Nat. Neurosci. 20:987–96
    [Google Scholar]
  19. Callaway EM. 2004. Feedforward, feedback and inhibitory connections in primate visual cortex. Neural. Netw. 17:625–32
    [Google Scholar]
  20. Campbell MJ, Lewis DA, Foote SL, Morrison JH 1987. Distribution of choline acetyltransferase-, serotonin-, dopamine-β-hydroxylase-, tyrosine hydroxylase-immunoreactive fibers in monkey primary auditory cortex. J. Comp. Neurol. 261:209–20
    [Google Scholar]
  21. Cappe C, Barone P. 2005. Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur. J. Neurosci. 22:2886–902
    [Google Scholar]
  22. Cauller L. 1995. Layer I of primary sensory neocortex: where top-down converges upon bottom-up. Behav. Brain Res. 71:163–70
    [Google Scholar]
  23. Cauller LJ, Clancy B, Connors BW 1998. Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J. Comp. Neurol. 390:297–310
    [Google Scholar]
  24. Cauller LJ, Connors BW. 1994. Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex. J. Neurosci. 14:751–62
    [Google Scholar]
  25. Cauller LJ, Kulics AT. 1988. A comparison of awake and sleeping cortical states by analysis of the somatosensory-evoked response of postcentral area 1 in rhesus monkey. Exp. Brain Res. 72:584–92
    [Google Scholar]
  26. Cauller LJ, Kulics AT. 1991. The neural basis of the behaviorally relevant N1 component of the somatosensory-evoked potential in SI cortex of awake monkeys: evidence that backward cortical projections signal conscious touch sensation. Exp. Brain Res. 84:607–19
    [Google Scholar]
  27. Chen Z, Wimmer RD, Wilson MA, Halassa MM 2015. Thalamic circuit mechanisms link sensory processing in sleep and attention. Front. Neural. Circuits 9:83
    [Google Scholar]
  28. Chittajallu R, Pelkey KA, McBain CJ 2013. Neurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation. Nat. Neurosci. 16:13–15
    [Google Scholar]
  29. Chou XL, Fang Q, Yan L, Zhong W, Peng B et al. 2020. Contextual and cross-modality modulation of auditory cortical processing through pulvinar mediated suppression. eLife9:e54157
    [Google Scholar]
  30. Chu Z, Galarreta M, Hestrin S 2003. Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23:96–102
    [Google Scholar]
  31. Cichon J, Gan WB. 2015. Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity. Nature 520:180–85
    [Google Scholar]
  32. Clasca F, Rubio-Garrido P, Jabaudon D 2012. Unveiling the diversity of thalamocortical neuron subtypes. Eur. J. Neurosci. 35:1524–32
    [Google Scholar]
  33. Clavagnier S, Falchier A, Kennedy H 2004. Long-distance feedback projections to area V1: implications for multisensory integration, spatial awareness, and visual consciousness. Cogn. Affect. Behav. Neurosci. 4:117–26
    [Google Scholar]
  34. Coogan TA, Burkhalter A. 1993. Hierarchical organization of areas in rat visual cortex. J. Neurosci. 13:3749–72
    [Google Scholar]
  35. Cruikshank SJ, Ahmed OJ, Stevens TR, Patrick SL, Gonzalez AN et al. 2012. Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32:17813–23
    [Google Scholar]
  36. de Lima AD, Bloom FE, Morrison JH 1988. Synaptic organization of serotonin-immunoreactive fibers in primary visual cortex of the macaque monkey. J. Comp. Neurol. 274:280–94
    [Google Scholar]
  37. DeFelipe J, Marco P, Busturia I, Merchan-Perez A 1999. Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb. Cortex 9:722–32
    [Google Scholar]
  38. Descarries L, Lemay B, Doucet G, Berger B 1987. Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 21:807–24
    [Google Scholar]
  39. Desimone R, Duncan J. 1995. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18:193–222
    [Google Scholar]
  40. Doron G, Shin JN, Takahashi N, Bocklisch C, Skenderi S et al. 2020. Perirhinal input to neocortical layer 1 controls learning. Science 370:eaaz3136
    [Google Scholar]
  41. Douglas RJ, Martin KA. 1991. A functional microcircuit for cat visual cortex. J. Physiol. 440:735–69
    [Google Scholar]
  42. Douglas RJ, Martin KA. 2004. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27:419–51
    [Google Scholar]
  43. D'Souza RD, Burkhalter A. 2017. A laminar organization for selective cortico-cortical communication. Front. Neuroanat. 11:71
    [Google Scholar]
  44. Emson PC, Koob GF. 1978. The origin and distribution of dopamine-containing afferents to the rat frontal cortex. Brain Res. 142:249–67
    [Google Scholar]
  45. Felleman DJ, Van Essen DC 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1:1–47
    [Google Scholar]
  46. Fiser A, Mahringer D, Oyibo HK, Petersen AV, Leinweber M, Keller GB 2016. Experience-dependent spatial expectations in mouse visual cortex. Nat. Neurosci. 19:1658–64
    [Google Scholar]
  47. Fitzpatrick KA, Imig TJ. 1980. Auditory cortico-cortical connections in the owl monkey. J. Comp. Neurol. 192:589–610
    [Google Scholar]
  48. Frick A, Johnston D. 2005. Plasticity of dendritic excitability. J. Neurobiol. 64:100–15
    [Google Scholar]
  49. Friedman DP. 1983. Laminar patterns of termination of cortico-cortical afferents in the somatosensory system. Brain Res. 273:147–51
    [Google Scholar]
  50. Friedman DP, Murray EA, O'Neill JB, Mishkin M 1986. Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J. Comp. Neurol. 252:323–47
    [Google Scholar]
  51. Friston K. 2018. Does predictive coding have a future?. Nat. Neurosci. 21:1019–21
    [Google Scholar]
  52. Fuxe K, Hamberger B, Hokfelt T 1968. Distribution of noradrenaline nerve terminals in cortical areas of the rat. Brain Res. 8:125–31
    [Google Scholar]
  53. Gambino F, Pages S, Kehayas V, Baptista D, Tatti R et al. 2014. Sensory-evoked LTP driven by dendritic plateau potentials in vivo. Nature 515:116–19
    [Google Scholar]
  54. Gao C, Leng Y, Ma J, Rooke V, Rodriguez-Gonzalez S et al. 2020. Two genetically, anatomically and functionally distinct cell types segregate across anteroposterior axis of paraventricular thalamus. Nat. Neurosci. 23:217–28
    [Google Scholar]
  55. Gharaei S, Honnuraiah S, Arabzadeh E, Stuart GJ 2020. Superior colliculus modulates cortical coding of somatosensory information. Nat. Commun. 11:1693
    [Google Scholar]
  56. Gilbert CD, Li W. 2013. Top-down influences on visual processing. Nat. Rev. Neurosci. 14:350–63
    [Google Scholar]
  57. Gilbert CD, Sigman M. 2007. Brain states: top-down influences in sensory processing. Neuron 54:677–96
    [Google Scholar]
  58. Golding NL, Staff NP, Spruston N 2002. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326–31
    [Google Scholar]
  59. Guillery RW. 1995. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J. Anat. 187:Pt. 3583–92
    [Google Scholar]
  60. Guo ZV, Inagaki HK, Daie K, Druckmann S, Gerfen CR, Svoboda K 2017. Maintenance of persistent activity in a frontal thalamocortical loop. Nature 545:181–86
    [Google Scholar]
  61. Halassa MM, Kastner S. 2017. Thalamic functions in distributed cognitive control. Nat. Neurosci. 20:1669–79
    [Google Scholar]
  62. Halassa MM, Sherman SM. 2019. Thalamocortical circuit motifs: a general framework. Neuron 103:762–70
    [Google Scholar]
  63. Harnett MT, Xu NL, Magee JC, Williams SR 2013. Potassium channels control the interaction between active dendritic integration compartments in layer 5 cortical pyramidal neurons. Neuron 79:516–29
    [Google Scholar]
  64. Harris JA, Mihalas S, Hirokawa KE, Whitesell JD, Choi H et al. 2019. Hierarchical organization of cortical and thalamic connectivity. Nature 575:195–202
    [Google Scholar]
  65. Häusser M, Spruston N, Stuart GJ 2000. Diversity and dynamics of dendritic signaling. Science 290:739–44
    [Google Scholar]
  66. He M, Tucciarone J, Lee S, Nigro MJ, Kim Y et al. 2016. Strategies and tools for combinatorial targeting of GABAergic neurons in mouse cerebral cortex. Neuron 91:1228–43
    [Google Scholar]
  67. Heeger DJ. 2017. Theory of cortical function. PNAS 114:1773–82
    [Google Scholar]
  68. Herkenham M. 1979. The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J. Comp. Neurol. 183:487–517
    [Google Scholar]
  69. Hestrin S, Armstrong WE. 1996. Morphology and physiology of cortical neurons in layer I. J. Neurosci. 16:5290–300
    [Google Scholar]
  70. Honjoh S, Sasai S, Schiereck SS, Nagai H, Tononi G, Cirelli C 2018. Regulation of cortical activity and arousal by the matrix cells of the ventromedial thalamic nucleus. Nat. Commun. 9:2100
    [Google Scholar]
  71. Hubel DH. 1982. Cortical neurobiology: a slanted historical perspective. Annu. Rev. Neurosci. 5:363–70
    [Google Scholar]
  72. Ibrahim LA, Huang S, Fernandez-Otero M, Sherer M, Vemuri S et al. 2021. Bottom-up inputs are required for the establishment of top-down connectivity onto cortical layer 1 neurogliaform cells. bioRxiv 2021.01.08.425944. https://doi.org/10.1101/2021.01.08.425944
    [Crossref]
  73. Ibrahim LA, Mesik L, Ji XY, Fang Q, Li HF et al. 2016. Cross-modality sharpening of visual cortical processing through layer-1-mediated inhibition and disinhibition. Neuron 89:1031–45
    [Google Scholar]
  74. Jarsky T, Roxin A, Kath WL, Spruston N 2005. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 8:1667–76
    [Google Scholar]
  75. Jiang X, Shen S, Cadwell CR, Berens P, Sinz F et al. 2015. Principles of connectivity among morphologically defined cell types in adult neocortex. Science 350:aac9462
    [Google Scholar]
  76. Jiang X, Wang G, Lee AJ, Stornetta RL, Zhu JJ 2013. The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16:210–18
    [Google Scholar]
  77. Jones EG. 2001. The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 24:595–601
    [Google Scholar]
  78. Jones EG. 2007. The Thalamus Cambridge, UK: Cambridge Univ. Press
  79. Jones EG. 2009. Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann. N. Y. Acad. Sci. 1157:10–23
    [Google Scholar]
  80. Juavinett AL, Callaway EM. 2015. Pattern and component motion responses in mouse visual cortical areas. Curr. Biol. 25:1759–64
    [Google Scholar]
  81. Kalmbach A, Hedrick T, Waters J 2012. Selective optogenetic stimulation of cholinergic axons in neocortex. J. Neurophysiol. 107:2008–19
    [Google Scholar]
  82. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M 2007. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10:743–53
    [Google Scholar]
  83. Kastner S, Ungerleider LG. 2000. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23:315–41
    [Google Scholar]
  84. Kayser C, Petkov CI, Augath M, Logothetis NK 2005. Integration of touch and sound in auditory cortex. Neuron 48:373–84
    [Google Scholar]
  85. Keller AJ, Roth MM, Scanziani M 2020. Feedback generates a second receptive field in neurons of the visual cortex. Nature 582:545–49
    [Google Scholar]
  86. Keller GB, Bonhoeffer T, Hubener M 2012. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 74:809–15
    [Google Scholar]
  87. Keller GB, Mrsic-Flogel TD. 2018. Predictive processing: a canonical cortical computation. Neuron 100:424–35
    [Google Scholar]
  88. Kerlin A, Mohar B, Flickinger D, MacLennan BJ, Dean MB et al. 2019. Functional clustering of dendritic activity during decision-making. eLife8:e46966
    [Google Scholar]
  89. Killackey H, Ebner F. 1973. Convergent projection of three separate thalamic nuclei on to a single cortical area. Science 179:283–85
    [Google Scholar]
  90. Kim EJ, Juavinett AL, Kyubwa EM, Jacobs MW, Callaway EM 2015. Three types of cortical layer 5 neurons that differ in brain-wide connectivity and function. Neuron 88:1253–67
    [Google Scholar]
  91. Kinomura S, Larsson J, Gulyas B, Roland PE 1996. Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 271:512–15
    [Google Scholar]
  92. Kosofsky BE, Molliver ME, Morrison JH, Foote SL 1984. The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey (Macaca fascicularis). J. Comp. Neurol. 230:168–78
    [Google Scholar]
  93. Krnjevic K, Silver A. 1965. A histochemical study of cholinergic fibres in the cerebral cortex. J. Anat. 99:711–59
    [Google Scholar]
  94. Kubota Y, Shigematsu N, Karube F, Sekigawa A, Kato S et al. 2011. Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb. Cortex 21:1803–17
    [Google Scholar]
  95. Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T 2009. Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb. Cortex 19:2065–77
    [Google Scholar]
  96. Kuramoto E, Pan S, Furuta T, Tanaka YR, Iwai H et al. 2017. Individual mediodorsal thalamic neurons project to multiple areas of the rat prefrontal cortex: a single neuron-tracing study using virus vectors. J. Comp. Neurol. 525:166–85
    [Google Scholar]
  97. Kuypers HG, Szwarcbart MK, Mishkin M, Rosvold HE 1965. Occipitotemporal corticocortical connections in the rhesus monkey. Exp. Neurol. 11:245–62
    [Google Scholar]
  98. Lacefield CO, Pnevmatikakis EA, Paninski L, Bruno RM 2019. Reinforcement learning recruits somata and apical dendrites across layers of primary sensory cortex. Cell Rep. 26:20008.e2
    [Google Scholar]
  99. Larkum M. 2013. A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex. Trends Neurosci. 36:141–51
    [Google Scholar]
  100. Larkum ME, Nevian T, Sandler M, Polsky A, Schiller J 2009. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325:756–60
    [Google Scholar]
  101. Larkum ME, Zhu JJ, Sakmann B 1999. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338–41
    [Google Scholar]
  102. Larkum ME, Zhu JJ, Sakmann B 2001. Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J. Physiol. 533:447–66
    [Google Scholar]
  103. Lee AJ, Wang G, Jiang X, Johnson SM, Hoang ET et al. 2015. Canonical organization of layer 1 neuron-led cortical inhibitory and disinhibitory interneuronal circuits. Cereb. Cortex 25:2114–26
    [Google Scholar]
  104. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B 2013. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16:1662–70
    [Google Scholar]
  105. Leinweber M, Ward DR, Sobczak JM, Attinger A, Keller GB 2017. A sensorimotor circuit in mouse cortex for visual flow predictions. Neuron 95:142032.e5
    [Google Scholar]
  106. Letzkus JJ, Kampa BM, Stuart GJ 2006. Learning rules for spike timing–dependent plasticity depend on dendritic synapse location. J. Neurosci. 26:10420–29
    [Google Scholar]
  107. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J et al. 2011. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480:331–35
    [Google Scholar]
  108. Levitt P, Moore RY. 1978. Noradrenaline neuron innervation of the neocortex in the rat. Brain Res. 139:219–31
    [Google Scholar]
  109. Lewis DA. 1991. Distribution of choline acetyltransferase-immunoreactive axons in monkey frontal cortex. Neuroscience 40:363–74
    [Google Scholar]
  110. Lewis DA, Campbell MJ, Foote SL, Goldstein M, Morrison JH 1987. The distribution of tyrosine hydroxylase-immunoreactive fibers in primate neocortex is widespread but regionally specific. J. Neurosci. 7:279–90
    [Google Scholar]
  111. Llinas R, Ribary U. 2001. Consciousness and the brain. The thalamocortical dialogue in health and disease. Ann. N. Y. Acad. Sci. 929:166–75
    [Google Scholar]
  112. Lorente de Nó R. 1938. The cerebral cortex. architecture. intracortical connections and motor projections. Physiology of the Nervous System J Fulton 291–339 London: Oxford Med. Publ.
    [Google Scholar]
  113. Losonczy A, Makara JK, Magee JC 2008. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452:436–41
    [Google Scholar]
  114. Lysakowski A, Wainer BH, Bruce G, Hersh LB 1989. An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex. Neuroscience 28:291–336
    [Google Scholar]
  115. Magee JC. 2000. Dendritic integration of excitatory synaptic input. Nat. Rev. Neurosci. 1:181–90
    [Google Scholar]
  116. Magee JC, Johnston D. 1997. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209–13
    [Google Scholar]
  117. Mago A, Weber JP, Ujfalussy BB, Makara JK 2020. Synaptic plasticity depends on the fine-scale input pattern in thin dendrites of CA1 pyramidal neurons. J. Neurosci. 40:2593–605
    [Google Scholar]
  118. Major G, Larkum ME, Schiller J 2013. Active properties of neocortical pyramidal neuron dendrites. Annu. Rev. Neurosci. 36:1–24
    [Google Scholar]
  119. Manita S, Suzuki T, Homma C, Matsumoto T, Odagawa M et al. 2015. A top-down cortical circuit for accurate sensory perception. Neuron 86:1304–16
    [Google Scholar]
  120. Marin-Padilla M. 1998. Cajal-Retzius cells and the development of the neocortex. Trends Neurosci. 21:64–71
    [Google Scholar]
  121. Marques T, Nguyen J, Fioreze G, Petreanu L 2018. The functional organization of cortical feedback inputs to primary visual cortex. Nat. Neurosci. 21:757–64
    [Google Scholar]
  122. Mashour GA. 2014. Top-down mechanisms of anesthetic-induced unconsciousness. Front. Syst. Neurosci. 8:115
    [Google Scholar]
  123. 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. 3:2563–86
    [Google Scholar]
  124. Mease RA, Metz M, Groh A 2016. Cortical sensory responses are enhanced by the higher-order thalamus. Cell Rep. 14:208–15
    [Google Scholar]
  125. Mechawar N, Cozzari C, Descarries L 2000. Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J. Comp. Neurol. 428:305–18
    [Google Scholar]
  126. Melzer S, Monyer H. 2020. Diversity and function of corticopetal and corticofugal GABAergic projection neurons. Nat. Rev. Neurosci. 21:499–515
    [Google Scholar]
  127. Meyer HS, Schwarz D, Wimmer VC, Schmitt AC, Kerr JN et al. 2011. Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. PNAS 108:16807–12
    [Google Scholar]
  128. Miller MW, Vogt BA. 1984. Direct connections of rat visual cortex with sensory, motor, and association cortices. J. Comp. Neurol. 226:184–202
    [Google Scholar]
  129. Mitchell BD, Cauller LJ. 2001. Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats. Brain Res. 921:68–77
    [Google Scholar]
  130. Morrison JH, Foote SL, Molliver ME, Bloom FE, Lidov HG 1982a. Noradrenergic and serotonergic fibers innervate complementary layers in monkey primary visual cortex: an immunohistochemical study. PNAS 79:2401–5
    [Google Scholar]
  131. Morrison JH, Foote SL, O'Connor D, Bloom FE 1982b. Laminar, tangential and regional organization of the noradrenergic innervation of monkey cortex: dopamine-β-hydroxylase immunohistochemistry. Brain Res. Bull. 9:309–19
    [Google Scholar]
  132. Morrissette AE, Chen PH, Bhamani C, Borden PY, Waiblinger C et al. 2019. Unilateral optogenetic inhibition and excitation of basal ganglia output affect directional lick choices and movement initiation in mice. Neuroscience 423:55–65
    [Google Scholar]
  133. Muñoz W, Tremblay R, Levenstein D, Rudy B 2017. Layer-specific modulation of neocortical dendritic inhibition during active wakefulness. Science 355:954–59
    [Google Scholar]
  134. Murayama M, Perez-Garci E, Nevian T, Bock T, Senn W, Larkum ME 2009. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457:1137–41
    [Google Scholar]
  135. Ohno S, Kuramoto E, Furuta T, Hioki H, Tanaka YR et al. 2012. A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb. Cortex 22:2840–57
    [Google Scholar]
  136. Oláh S, Fule M, Komlosi G, Varga C, Baldi R et al. 2009. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461:1278–81
    [Google Scholar]
  137. Oswald AM, Doiron B, Rinzel J, Reyes AD 2009. Spatial profile and differential recruitment of GABAB modulate oscillatory activity in auditory cortex. J. Neurosci. 29:10321–34
    [Google Scholar]
  138. Overstreet-Wadiche L, McBain CJ. 2015. Neurogliaform cells in cortical circuits. Nat. Rev. Neurosci. 16:458–68
    [Google Scholar]
  139. Palmer LM, Schulz JM, Murphy SC, Ledergerber D, Murayama M, Larkum ME 2012. The cellular basis of GABAB-mediated interhemispheric inhibition. Science 335:989–93
    [Google Scholar]
  140. Palmer LM, Shai AS, Reeve JE, Anderson HL, Paulsen O, Larkum ME 2014. NMDA spikes enhance action potential generation during sensory input. Nat. Neurosci. 17:383–90
    [Google Scholar]
  141. Pandya DN, Dye P, Butters N 1971. Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey. Brain Res. 31:35–46
    [Google Scholar]
  142. Pandya DN, Kuypers HG. 1969. Cortico-cortical connections in the rhesus monkey. Brain Res. 13:13–36
    [Google Scholar]
  143. Pandya DN, Rosene DL. 1993. Laminar termination patterns of thalamic, callosal, and association afferents in the primary auditory area of the rhesus monkey. Exp. Neurol. 119:220–34
    [Google Scholar]
  144. Pandya DN, Sanides F. 1973. Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern. Z. Anat. Entwicklungsgesch. 139:127–61
    [Google Scholar]
  145. Petreanu L, Mao T, Sternson SM, Svoboda K 2009. The subcellular organization of neocortical excitatory connections. Nature 457:1142–45
    [Google Scholar]
  146. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M 2013. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16:1068–76
    [Google Scholar]
  147. Polsky A, Mel BW, Schiller J 2004. Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 7:621–27
    [Google Scholar]
  148. Price CJ, Scott R, Rusakov DA, Capogna M 2008. GABAB receptor modulation of feedforward inhibition through hippocampal neurogliaform cells. J. Neurosci. 28:6974–82
    [Google Scholar]
  149. Pronneke A, Scheuer B, Wagener RJ, Mock M, Witte M, Staiger JF 2015. Characterizing VIP neurons in the barrel cortex of VIPcre/tdTomato mice reveals layer-specific differences. Cereb. Cortex 25:4854–68
    [Google Scholar]
  150. Purushothaman G, Marion R, Li K, Casagrande VA 2012. Gating and control of primary visual cortex by pulvinar. Nat. Neurosci. 15:905–12
    [Google Scholar]
  151. Rao RP, Ballard DH. 1999. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2:79–87
    [Google Scholar]
  152. Rockland KS, Ojima H. 2003. Multisensory convergence in calcarine visual areas in macaque monkey. Int. J. Psychophysiol. 50:19–26
    [Google Scholar]
  153. Rockland KS, Pandya DN. 1979. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179:3–20
    [Google Scholar]
  154. Roth MM, Dahmen JC, Muir DR, Imhof F, Martini FJ, Hofer SB 2016. Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex. Nat. Neurosci. 19:299–307
    [Google Scholar]
  155. Rubio-Garrido P, Perez-de-Manzo F, Porrero C, Galazo MJ, Clasca F 2009. Thalamic input to distal apical dendrites in neocortical layer 1 is massive and highly convergent. Cereb. Cortex 19:2380–95
    [Google Scholar]
  156. Saalmann YB, Pinsk MA, Wang L, Li X, Kastner S 2012. The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337:753–56
    [Google Scholar]
  157. Scannell JW, Blakemore C, Young MP 1995. Analysis of connectivity in the cat cerebral cortex. J. Neurosci. 15:1463–83
    [Google Scholar]
  158. Schmitt LI, Wimmer RD, Nakajima M, Happ M, Mofakham S, Halassa MM 2017. Thalamic amplification of cortical connectivity sustains attentional control. Nature 545:219–23
    [Google Scholar]
  159. Schneider DM, Mooney R. 2018. How movement modulates hearing. Annu. Rev. Neurosci. 41:553–72
    [Google Scholar]
  160. Schneider DM, Nelson A, Mooney R 2014. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513:189–94
    [Google Scholar]
  161. Schuman B, Machold RP, Hashikawa Y, Fuzik J, Fishell GJ, Rudy B 2019. Four unique interneuron populations reside in neocortical layer 1. J. Neurosci. 39:125–39
    [Google Scholar]
  162. Schwiedrzik CM, Freiwald WA. 2017. High-level prediction signals in a low-level area of the macaque face-processing hierarchy. Neuron 96:8997.e4
    [Google Scholar]
  163. Sherman SM, Guillery RW. 2005. Exploring the Thalamus and Its Role in Cortical Function Cambridge, MA: MIT Press
  164. Shipp S, Zeki S. 1989. The organization of connections between areas V5 and V2 in macaque monkey visual cortex. Eur. J. Neurosci. 1:333–54
    [Google Scholar]
  165. Silberberg G, Markram H. 2007. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53:735–46
    [Google Scholar]
  166. Sjöström PJ, Häusser M. 2006. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 51:227–38
    [Google Scholar]
  167. Spatz WB. 1977. Topographically organized reciprocal connections between areas 17 and MT (visual area of superior temporal sulcus) in the marmoset Callithrix jacchus. Exp. Brain Res. 27:559–72
    [Google Scholar]
  168. Stanley J, Miall RC. 2007. Functional activation in parieto-premotor and visual areas dependent on congruency between hand movement and visual stimuli during motor-visual priming. Neuroimage 34:290–99
    [Google Scholar]
  169. Stehberg J, Dang PT, Frostig RD 2014. Unimodal primary sensory cortices are directly connected by long-range horizontal projections in the rat sensory cortex. Front. Neuroanat. 8:93
    [Google Scholar]
  170. Stepanyants A, Martinez LM, Ferecsko AS, Kisvarday ZF 2009. The fractions of short- and long-range connections in the visual cortex. PNAS 106:3555–60
    [Google Scholar]
  171. Steriade M. 1996. Awakening the brain. Nature 383:24–25
    [Google Scholar]
  172. Steriade M, Jones EG, Llinás RR 1990. Thalamic Oscillations and Signaling New York: Wiley
  173. Stuart G, Spruston N. 1998. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18:3501–10
    [Google Scholar]
  174. Stuart GJ, Spruston N. 2015. Dendritic integration: 60 years of progress. Nat. Neurosci. 18:1713–21
    [Google Scholar]
  175. Stuart G, Spruston N, Sakmann B, Hausser M 1997. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20:125–31
    [Google Scholar]
  176. Suzuki M, Larkum ME. 2020. General anesthesia decouples cortical pyramidal neurons. Cell 180:66676.e13
    [Google Scholar]
  177. Takahashi H, Magee JC. 2009. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 62:102–11
    [Google Scholar]
  178. Takahashi N, Ebner C, Sigl-Glockner J, Moberg S, Nierwetberg S, Larkum ME 2020. Active dendritic currents gate descending cortical outputs in perception. Nat. Neurosci. 23:1277–85
    [Google Scholar]
  179. Takahashi N, Oertner TG, Hegemann P, Larkum ME 2016. Active cortical dendrites modulate perception. Science 354:1587–90
    [Google Scholar]
  180. Tamas G, Lorincz A, Simon A, Szabadics J 2003. Identified sources and targets of slow inhibition in the neocortex. Science 299:1902–5
    [Google Scholar]
  181. Tanaka YH, Tanaka YR, Kondo M, Terada SI, Kawaguchi Y, Matsuzaki M 2018. Thalamocortical axonal activity in motor cortex exhibits layer-specific dynamics during motor learning. Neuron 100:24458.e12
    [Google Scholar]
  182. Thierry AM, Blanc G, Sobel A, Stinus L, Glowinski J 1973. Dopaminergic terminals in the rat cortex. Science 182:499–501
    [Google Scholar]
  183. Tigges J, Spatz WB, Tigges M 1973. Reciprocal point-to-point connections between parastriate and striate cortex in the squirrel monkey (Saimiri). J. Comp. Neurol. 148:481–89
    [Google Scholar]
  184. Tremblay R, Lee S, Rudy B 2016. GABAergic interneurons in the neocortex: from cellular properties to circuits. Neuron 91:260–92
    [Google Scholar]
  185. Urban-Ciecko J, Fanselow EE, Barth AL 2015. Neocortical somatostatin neurons reversibly silence excitatory transmission via GABAb receptors. Curr. Biol. 25:722–31
    [Google Scholar]
  186. Van der Werf YD, Witter MP, Groenewegen HJ 2002. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Rev. 39:107–40
    [Google Scholar]
  187. Vicente R, Gollo LL, Mirasso CR, Fischer I, Pipa G 2008. Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays. PNAS 105:17157–62
    [Google Scholar]
  188. Vogt BA, Pandya DN. 1987. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J. Comp. Neurol. 262:271–89
    [Google Scholar]
  189. Wang X, Tucciarone J, Jiang S, Yin F, Wang BS et al. 2019. Genetic single neuron anatomy reveals fine granularity of cortical axo-axonic cells. Cell Rep. 26:314559.e5
    [Google Scholar]
  190. Weber JP, Andrasfalvy BK, Polito M, Mago A, Ujfalussy BB, Makara JK 2016. Location-dependent synaptic plasticity rules by dendritic spine cooperativity. Nat. Commun. 7:11380
    [Google Scholar]
  191. Williams LE, Holtmaat A. 2019. Higher-order thalamocortical inputs gate synaptic long-term potentiation via disinhibition. Neuron 101:91102.e4
    [Google Scholar]
  192. Williams SR, Stuart GJ. 2002. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295:1907–10
    [Google Scholar]
  193. Wilson MA, Molliver ME. 1991. The organization of serotonergic projections to cerebral cortex in primates: regional distribution of axon terminals. Neuroscience 44:537–53
    [Google Scholar]
  194. Wong-Riley M. 1979. Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys. Brain Res. 162:201–17
    [Google Scholar]
  195. Wozny C, Williams SR. 2011. Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb. Cortex 21:1818–26
    [Google Scholar]
  196. Xu H, Jeong H-Y, Tremblay R, Rudy B 2013. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77:155–67
    [Google Scholar]
  197. Xu NL, Harnett MT, Williams SR, Huber D, O'Connor DH et al. 2012. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492:247–51
    [Google Scholar]
  198. Xu X, Roby KD, Callaway EM 2010. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518:389–404
    [Google Scholar]
  199. Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M 2012. The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48:58–81
    [Google Scholar]
  200. Zagha E. 2020. Shaping the cortical landscape: functions and mechanisms of top-down cortical feedback pathways. Front. Syst. Neurosci. 14:33
    [Google Scholar]
  201. Zhang S, Xu M, Kamigaki T, Hoang Do JP, Chang WC et al. 2014. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345:660–65
    [Google Scholar]
  202. Zhang W, Bruno RM. 2019. High-order thalamic inputs to primary somatosensory cortex are stronger and longer lasting than cortical inputs. eLife8:e44158
    [Google Scholar]
  203. Zhou FM, Hablitz JJ. 1996. Morphological properties of intracellularly labeled layer I neurons in rat neocortex. J. Comp. Neurol. 376:198–213
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-100520-012117
Loading
/content/journals/10.1146/annurev-neuro-100520-012117
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error