1932

Abstract

The claustrum is one of the most widely connected regions of the forebrain, yet its function has remained obscure, largely due to the experimentally challenging nature of targeting this small, thin, and elongated brain area. However, recent advances in molecular techniques have enabled the anatomy and physiology of the claustrum to be studied with the spatiotemporal and cell type–specific precision required to eventually converge on what this area does. Here we review early anatomical and electrophysiological results from cats and primates, as well as recent work in the rodent, identifying the connectivity, cell types, and physiological circuit mechanisms underlying the communication between the claustrum and the cortex. The emerging picture is one in which the rodent claustrum is closely tied to frontal/limbic regions and plays a role in processes, such as attention, that are associated with these areas.

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2020-07-08
2024-03-29
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Literature Cited

  1. Ährlund-Richter S, Xuan Y, van Lunteren JA, Kim H, Ortiz C et al. 2019. A whole-brain atlas of monosynaptic input targeting four different cell types in the medial prefrontal cortex of the mouse. Nat. Neurosci. 22:657–68
    [Google Scholar]
  2. Ashwell KW, Hardman C, Paxinos G 2004. The claustrum is not missing from all monotreme brains. Brain. Behav. Evol. 64:4223–41
    [Google Scholar]
  3. Atlan G, Terem A, Peretz-Rivlin N, Groysman M, Citri A 2017. Mapping synaptic cortico-claustral connectivity in the mouse. J. Comp. Neurol. 525:1381–402
    [Google Scholar]
  4. Atlan G, Terem A, Peretz-Rivlin N, Sehrawat K, Gonzales BJ et al. 2018. The claustrum supports resilience to distraction. Curr. Biol. 28:172752–62
    [Google Scholar]
  5. Baizer JS. 2001. Serotonergic innervation of the primate claustrum. Brain. Res. Bull. 55:3431–34
    [Google Scholar]
  6. Baizer JS, Sherwood CC, Noonan M, Hof PR 2014. Comparative organization of the claustrum: What does structure tell us about function. ? Front. Syst. Neurosci. 8:117
    [Google Scholar]
  7. Behan M, Haberly LB. 1999. Intrinsic and efferent connections of the endopiriform nucleus in rat. J. Comp. Neurol. 408:532–48
    [Google Scholar]
  8. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8:1263–68
    [Google Scholar]
  9. Brown SP, Hestrin S. 2009. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457:1133–36
    [Google Scholar]
  10. Butler AB, Molnar Z, Manger PR 2012. Apparent absence of claustrum in monotremes: implications for forebrain evolution in amniotes. Brain Behav. Evol. 60:4230–40
    [Google Scholar]
  11. Chia Z, Silberberg G, Augustine GJ 2017. Functional properties, topological organization and sexual dimorphism of claustrum neurons projecting to anterior cingulate cortex. Claustrum 2:1 https://doi.org/10.1080/20023294.2017.1357412
    [Crossref] [Google Scholar]
  12. Cortimiglia R, Crescimanno G, Salerno MT, Amato G 1991. The role of the claustrum in the bilateral control of frontal oculomotor neurons in the cat. Exp. Brain Res. 84:471–77
    [Google Scholar]
  13. Crescimanno G, Salerno MT, Cortimiglia R, Amato G 1989. Claustral influence on ipsi- and contralateral motor cortical areas, in the cat. Brain Res. Bull. 22:839–43
    [Google Scholar]
  14. Crescimanno G, Salerno MT, Cortimiglia R, Amato G 1990. Effect of claustrum stimulation on neurons of the contralateral medial oculomotor area, in the cat. Neurosci. Lett. 114:289–94
    [Google Scholar]
  15. Crick FC, Koch C. 2005. What is the function of the claustrum. ? Phil. Trans. Roy. Soc. B. 360:1271–79
    [Google Scholar]
  16. da Costa NM, Fursinger D, Martin KAC 2010. The synaptic organization of the claustral projection to the cat's visual cortex. J. Neurosci. 30:13166–70
    [Google Scholar]
  17. Diekelmann S, Born J. 2010. The memory function of sleep. Nat. Rev. Neurosci. 11:2114–26
    [Google Scholar]
  18. Delevich K, Tucciarone J, Huang ZJ, Li B 2015. The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J. Neurosci. 35:5743–53
    [Google Scholar]
  19. Deuchars J, Thomson AM. 1996. CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74:1009–18
    [Google Scholar]
  20. Dilgen J, Tejeda HA, O'Donnell P 2013. Amygdala inputs drive feedforward inhibition in the medial prefrontal cortex. J. Neurophysiol. 110:221–29
    [Google Scholar]
  21. Dillingham CM, Mathiasen ML, Frost BE, Lambert MAC, Bubb EJ et al. 2019. The anatomical boundary of the rat claustrum. Front. Neuroanat. 13:53
    [Google Scholar]
  22. Edelstein LR, Denaro FJ. 2004. The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell. Molec. Biol. 50:6675–702
    [Google Scholar]
  23. Eiden LE, Mezey É, Eskay RL, Beinfeld MC, Palkovits M 1990. Neuropeptide content and connectivity of the rat claustrum. Brain Res 523:245–50
    [Google Scholar]
  24. Fernandez-Miranda JC, Rhoton AL, Kakizawa Y, Choi C, Alvarex-Linera J 2008. The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J. Neurosurg. 108:764–74
    [Google Scholar]
  25. Floresco SB, Tse MT. 2007. Dopaminergic regulation of inhibitory and excitatory transmission in the basolateral amygdala-prefrontal cortical pathway. J. Neurosci. 27:2045–57
    [Google Scholar]
  26. Goll Y, Atlan G, Citri A 2015. Attention: the claustrum. Trends Neurosci 38:8486–95
    [Google Scholar]
  27. Gozzi A, Schwarz AJ. 2016. Large-scale functional connectivity networks in the rodent brain. Neuroimage 127:496–509
    [Google Scholar]
  28. Guirado S, Real , Olmos JL, Dávila JC 2003. Distinct types of nitric oxide-producing neurons in the developing and adult mouse claustrum. J. Comp. Neurol. 465:431–44
    [Google Scholar]
  29. Hadjikhani N, Roland PE. 1998. Cross-modal transfer of information between the tactile and the visual representations in the human brain: a positron emission tomographic study. J. Neurosci. 18:31072–84
    [Google Scholar]
  30. Higley MJ, Contreras D. 2006. Balanced excitation and inhibition determine spike timing during frequency adaptation. J. Neurosci. 26:448–57
    [Google Scholar]
  31. Holmgren C, Harkany T, Svennenfors B, Zilberter Y 2003. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. 551:139–53
    [Google Scholar]
  32. Hong CCH, Harris JC, Pearlson GD, Kim JS, Calhoun VD et al. 2009. FMRI evidence for multisensory recruitment associated with rapid eye movements during sleep. Hum. Brain Mapp. 30:1705–22
    [Google Scholar]
  33. Jackson J, Karnani MM, Zemelman BV, Burdakov D, Lee AK 2018. Inhibitory control of prefrontal cortex by claustrum. Neuron 99:51029–39
    [Google Scholar]
  34. Jankowski MM, O'Mara SM. 2015. Dynamics of place, boundary and object encoding in rat anterior claustrum. Front. Behav. Neurosci. 9:250
    [Google Scholar]
  35. Ji D, Wilson MA. 2007. Coordinated replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10:100–7
    [Google Scholar]
  36. Kim J, Matney CJ, Roth RH, Brown SP 2016. Synaptic organization of the neuronal circuits of the claustrum. J. Neurosci. 36:3773–84
    [Google Scholar]
  37. Kitamura T, Ogawa SK, Roy DS, Okuyama T, Morrissey MD et al. 2017. wEngrams and circuits crucial for systems consolidation of a memory. Science 356:633373–78
    [Google Scholar]
  38. Kitanishi T, Matsuo N. 2017. Organization of the claustrum-to-entorhinal cortical connection in mice. J. Neurosci. 37:2269–80
    [Google Scholar]
  39. Ko H, Cossell L, Baragli C, Antolik J, Clopath C et al. 2013. The emergence of functional microcircuits in visual cortex. Nature 496:96–100
    [Google Scholar]
  40. Koubeissi MZ, Barolomei F, Beltagy A, Picard F 2014. Electrical stimulation of a small brain area reversibly disrupts consciousness. Epilepsy Behav 37:32–35
    [Google Scholar]
  41. Kowiański P, Dziewiatkowski J, Kowiańska J, Moryś J 1999. Comparative anatomy of the claustrum in selected species: a morphometric analysis. Brain Behav. Evol. 53:44–54
    [Google Scholar]
  42. Krimmel SR, Qadir H, Hesselgrave N, White MG, Reser DH, Mathur BN, Seminowicz DA 2019a. Resting state functional connectivity of the rat claustrum. Front. Neuroanat. 13:22
    [Google Scholar]
  43. Krimmel SR, White MG, Panicker MH, Barrett FS, Mathur BN, Seminowicz DA 2019b. Resting state functional connectivity and cognitive task-related activation of the human claustrum. Neuroimage 196:59–67
    [Google Scholar]
  44. Lee AK, Wilson MA. 2002. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:61183–94
    [Google Scholar]
  45. LeVay S. 1986. Visual cortex: what layer 6 tells layer 4. Nature 320:6060310–11
    [Google Scholar]
  46. LeVay S, Sherk H. 1981a. The visual claustrum of the cat. I. Structure and connections. J. Neurosci. 1:9956–80
    [Google Scholar]
  47. LeVay S, Sherk H. 1981b. The visual claustrum of the cat. II. The visual field map. J. Neurosci. 1:9981–92
    [Google Scholar]
  48. LeVay S, Sherk H. 1981c. The visual claustrum of the cat. III. Receptive field properties. J. Neurosci. 1:9993–1002
    [Google Scholar]
  49. LeVay S, Sherk H. 1981d. Visual claustrum: topography and receptive field properties in the cat. Science 212:449087–89
    [Google Scholar]
  50. Louie K, Wilson MA. 2001. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–56
    [Google Scholar]
  51. Majak K, Pikkarainen M, Kemppainen S, Jolkkonen E, Pitkanen A 2002. Projections from the amygdaloid complex to the claustrum and the endopiriform nucleus: a Phaseoulus vulgaris leucoagglutinin study in the rat. J. Comp. Neurol. 451:236–49
    [Google Scholar]
  52. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, Watson SJ 1994. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350:412–38
    [Google Scholar]
  53. Marek R, Jin J, Goode TD, Giustino TF, Wang Q et al. 2018. Hippocampus-driven feed-forward inhibition of the prefrontal cortex mediates relapse of extinguished fear. Nat. Neurosci. 21:384–92
    [Google Scholar]
  54. Marshall L, Helgadóttir H, Mölle M, Born J 2006. Boosting slow oscillations during sleep potentiates memory. Nature 444:7119610–13
    [Google Scholar]
  55. Mathur BN. 2014. The claustrum in review. Front. Syst. Neurosci. 8:48
    [Google Scholar]
  56. Mathur BN, Caprioli RM, Deutch AY 2009. Proteomic analysis illuminates a novel structural definition of the claustrum and insula. Cereb. Cortex 19:102372–79
    [Google Scholar]
  57. McGarry LM, Carter AG. 2016. Inhibitory gating of basolateral amygdala inputs to the prefrontal cortex. J. Neurosci. 36:9391–406
    [Google Scholar]
  58. Menon V. 2011. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. 15:483–506
    [Google Scholar]
  59. Milardi D, Bramanti P, Milazzo C, Finocchio G, Arrigo A et al. 2013. Cortical and subcortical connections of the human claustrum revealed in vivo by constrained spherical deconvolution tractography. Cereb. Cortex 25:2406–14
    [Google Scholar]
  60. Minciacchi D, Molinari M, Bentivoglio M, Macchi G 1985. The organization of the ipsi- and contralateral claustrocortical system in rat with notes on the bilateral claustrocortical projections in cat. Neurosci 16:3557–76
    [Google Scholar]
  61. Narikiyo K, Mizuguchi R, Ajima A, Mitsui S, Shiozaki M et al. 2018. The claustrum coordinates cortical slow-wave activity. bioRxiv 286773. https://doi.org/10.1101/286773
    [Crossref]
  62. Norimoto H, Fenk LA, Li H-H, Tosches MA, Gallego-Flores T et al. 2020. A claustrum in reptiles and its role in slow-wave sleep. Nature https://doi.org/10.1038/s41586-020-1993-6
    [Google Scholar]
  63. Oh SW, Harris JA, Ng L, Winslow B, Cain N et al. 2014. A mesoscale connectome of the mouse brain. Nature 508:207–14
    [Google Scholar]
  64. Olson CR, Graybiel AM. 1980. Sensory maps in the claustrum of the cat. Nature 288:5790479–81
    [Google Scholar]
  65. Orman R. 2015. Claustrum: a case for directional, excitatory, intrinsic connectivity in the rat. J. Physiol. Sci. 65:6533–44
    [Google Scholar]
  66. Parent A. 2012. The history of the basal ganglia: the contribution of Karl Friedrich Burdach. Neurosci. Med. 3:4374–79
    [Google Scholar]
  67. Pearson RC, Brodal P, Gatter KC, Powell TP 1982. The organization of the connections between the cortex and the claustrum in the monkey. Brain Res 234:2435–41
    [Google Scholar]
  68. Pompeiano M, Cirelli C, Tononi G 1994. Immediate‐early genes in spontaneous wakefulness and sleep: expression of c‐fos and NGFI‐A mRNA and protein. J. Sleep Res. 3:80–96
    [Google Scholar]
  69. Pouille F, Scanziani M. 2001. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:55321159–63
    [Google Scholar]
  70. Ptito M, Lassonde MC. 1981. Effects of claustral stimulation on the properties of visual cortex neurons in the cat. Exp. Neurol. 73:315–20
    [Google Scholar]
  71. Puelles L, Yad A, Alonso A, Sandoval JE, Martinez-de-la-Torre M et al. 2016. Selective early expression of the orphan nuclear receptor Nr4a2 identifies the claustrum homolog in the avian mesopallium: impact on sauropsidian/mammalian pallium comparisons. J. Comp. Neurol. 524:665–703
    [Google Scholar]
  72. Remedios R, Logothetis NK, Kayser C 2010. Unimodal responses prevail within the multisensory claustrum. J. Neurosci. 30:3912902–7
    [Google Scholar]
  73. Remedios R, Logothetis NK, Kayser C 2014. A role of the claustrum in auditory scene analysis by reflecting sensory change. Front. Syst. Neurosci. 8:44
    [Google Scholar]
  74. Renouard L, Billwiller F, Ogawa K, Clement O, Camargo N et al. 2015. The supramammillary nucleus and the claustrum activate the cortex during REM sleep. Sci. Adv. 1:e1400177
    [Google Scholar]
  75. Salerno MT, Cortimiglia R, Crescimanno G, Amato G 1989. Effect of claustrum activation on the spontaneous unitary activity of frontal eye field neurons in the cat. Neurosci. Lett. 98:299–304
    [Google Scholar]
  76. Salerno MT, Cortimiglia R, Crescimanno G, Amato G, Infantellina F 1984. Effects of claustrum stimulation on spontaneous bioelectrical activity of motor cortex neurons in the cat. Exp. Neurol. 86:227–39
    [Google Scholar]
  77. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH et al. 2007. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27:92349–56
    [Google Scholar]
  78. Sforazzini F, Schwarz AJ, Galbusera A, Bifone A, Gozzi A 2014. Distributed BOLD and CBV-weighted resting-state networks in the mouse brain. Neuroimage 87:403–15
    [Google Scholar]
  79. Shepherd GMG 2013. Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14:4278–91
    [Google Scholar]
  80. Sherk H. 1986. The claustrum and the cerebral cortex. Sensory-Motor Areas and Aspects of Cortical Connectivity EG Jones, A Peters 467–99 New York, NY: Plenum
    [Google Scholar]
  81. Sherk H, LeVay S. 1983. Contribution of the cortico-claustral loop to receptive field properties in area 17 of the cat. J. Neurosci. 3:112121–27
    [Google Scholar]
  82. Shibuya H, Yamamoto T. 1998. Electrophysiological and morphological features of rat claustral neurons: an intracellular staining study. Neuroscience 85:41037–49
    [Google Scholar]
  83. Shima K, Hoshi E, Tanji J 1996. Neuronal activity in the claustrum of the monkey during performance of multiple movements. J. Neurophysiol. 76:32115–19
    [Google Scholar]
  84. Sitte HH, Pifl C, Rajput AH, Hortnag H, Tong J et al. 2017. Dopamine and noradrenaline, but not serotonin, in the human claustrum are greatly reduced in patients with Parkinson's disease: possible functional implications. Eur. J. Neurosci. 45:1192–97
    [Google Scholar]
  85. Smith JB, Alloway KD. 2010. Functional specificity of claustrum connections in the rat: interhemispheric communication between specific parts of motor cortex. J. Neurosci. 518:224546–66
    [Google Scholar]
  86. Smith JB, Alloway KD. 2014. Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Front. Syst. Neurosci. 8:93
    [Google Scholar]
  87. Smith JB, Alloway KD, Hof PR, Orman R, Reser DH et al. 2018. The relationship between the claustrum and endopiriform nucleus: a perspective towards consensus on cross-species homology. J. Comp. Neurol. 527:2476–99
    [Google Scholar]
  88. Smith JB, Klug JR, Ross DL, Howard CD, Hollon NG et al. 2016. Genetic-based dissection unveils the inputs and outputs of striatal patch and matrix compartments. Neuron 91:51069–84
    [Google Scholar]
  89. Smith JB, Liang Z, Watson GDW, Alloway KD, Zhang N 2017. Interhemispheric resting-state functional connectivity of the claustrum in the awake and anesthetized states. Brain Struct. Func. 222:52041–58
    [Google Scholar]
  90. Smith JB, Radhakrishnan H, Alloway KD 2012. Rat claustrum coordinates but does not integrate somatosensory and motor cortical information. J. Neurosci. 32:258583–88
    [Google Scholar]
  91. Smith JB, Watson GDW, Liang Z, Liu Y, Zhang N, Alloway KD 2019. A role for the claustrum in salience processing. ? Front. Neuroanat. 13:64
    [Google Scholar]
  92. Smythies J, Edelstein L, Ramachandran V 2012. Hypotheses relating to the function of the claustrum. Front. Integr. Neurosci. 6:53
    [Google Scholar]
  93. Stark E, Roux L, Eichler R, Senzai Y, Royer S, Buzsaki G 2014. Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83:2467–80
    [Google Scholar]
  94. Sternson SM, Roth BL. 2014. Chemogenetic tools to interrogate brain functions. Annu. Rev. Neurosci. 37:387–407
    [Google Scholar]
  95. Stiefel KM, Merrifield A, Holcombe AO 2014. The claustrum's proposed role in consciousness is supported by the effect and target localization of Salvia divinorum. Front. Integr. . Neurosci 8:20
    [Google Scholar]
  96. Suarez R, Paolino A, Fenlon LR, Morcom LR, Kozulin P et al. 2018. A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum. PNAS 115:389622–27
    [Google Scholar]
  97. Tervo DGR, Hwang BY, Viswanathan S, Gaj T, Lavzin M et al. 2016. A designer AAV variant permits efficient retrograde access to projection neurons. Neuron 92:372–82
    [Google Scholar]
  98. Torgerson CM, Irimia A, Goh SY, Van Horn JD 2015. The DTI connectivity of the human claustrum. Hum. Brain Mapp. 36:3827–38
    [Google Scholar]
  99. Tsumoto T, Suda K. 1982. Effects of stimulation of the dorsocaudal claustrum on activities of striate cortex neurons in the cat. Brain Res 240:345–49
    [Google Scholar]
  100. Wang Q, Ng L, Harris JA, Feng D, Li Y et al. 2017. Organization of the connections between the claustrum and cortex in the mouse. J. Comp. Neurol. 525:61317–46
    [Google Scholar]
  101. Wang Y, Xie P, Gong H, Zhou Z, Kuang X et al. 2019. Complete single neuron reconstruction reveals morphological diversity in molecularly defined claustral and cortical neuron types. bioRxiv 675280. https://doi.org/10.1101/675280
    [Crossref]
  102. Watson GDW, Smith JB, Alloway KD 2017. Interhemispheric connections between the infralimbic and entorhinal cortices: The endopiriform nucleus has limbic connections that parallel the sensory and motor connections of the claustrum. J. Comp. Neurol. 525:61363–80
    [Google Scholar]
  103. White MG, Cody PA, Bubser M, Wang HD, Deutch AY et al. 2017. Cortical hierarchy governs rat claustrocortical circuit organization. J. Comp. Neurol. 525:61347–62
    [Google Scholar]
  104. White MG, Mathur BN. 2018. Frontal cortical control of posterior sensory and association cortices through the claustrum. Brain Struct. Func. 223:62999–3006
    [Google Scholar]
  105. White MG, Panicker M, Mu C, Carter AM, Roberts BM et al. 2018. Anterior cingulate cortex input to the claustrum is required for top-down action control. Cell Rep 22:184–95
    [Google Scholar]
  106. Wilson MA, McNaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265:676–79
    [Google Scholar]
  107. Winnubst J, Bas E, Ferreira TA, Wu Z, Economo MN et al. 2019. Reconstruction of 1,000 projection neurons reveals new cell types and organization of long-range connectivity in the mouse brain. Cell 179:268–81.e13
    [Google Scholar]
  108. Yagaloff KA, Hartig PR. 1985. 125I-Lysergic acid diethylamide binds to a novel serotonergic site on rat choroid plexus epithelial cells. J. Comp. Neurol. 5:123178–83
    [Google Scholar]
  109. Zingg B, Dong HW, Tao HW, Zhang LI 2018. Input-output organization of the mouse claustrum. J. Comp. Neurol. 526:152428–43
    [Google Scholar]
  110. Zingg B, Hintiryan H, Gou L, Song MY, Bay M et al. 2014. Neural networks of the mouse neocortex. Cell 156:1096–111
    [Google Scholar]
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