Abstract
Anterior cingulate cortex (ACC) input to the claustrum is required for top–down cognitive control of action. By virtue of its widespread cortical connectivity, the claustrum is anatomically situated to process and broadcast top–down signals from ACC to downstream cortices. To gain a deeper understanding of claustrum processing mechanisms, it is first critical to identify the projection neuron subtypes within claustrum, the intrinsic and extrinsic components regulating their firing, and the differential innervation of cortex by projection neuron subtypes. To this end, we used whole-cell patch-clamp electrophysiology in adult mouse brain slices to distinguish two spiny projection neuron subtypes in claustrum, referred to as type I and II neurons, and three aspiny interneuron subtypes, referred to as type III, IV, and V neurons. In response to optogenetic ACC afferent stimulation, type II neurons preferentially burst fire relative to type I neurons. This burst firing is calcium-dependent and is optimized by voltage-gated potassium channels. Finally, we find that visual cortices, parietal association cortex, and ACC receive input from type I and II neurons in differing proportions. These data reveal the diversity of claustrum neurons and mechanisms by which claustrum processes ACC command for spatiotemporal coordination of the cerebral cortex.
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References
Arlotta P, Molyneaux BJ, Chen J et al (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:207–221. https://doi.org/10.1016/j.neuron.2004.12.036
Atlan G, Terem A, Peretz-Rivlin N et al (2017) Mapping synaptic cortico-claustral connectivity in the mouse. J Comp Neurol 525:1381–1402. https://doi.org/10.1002/cne.23997
Atwood BK, Kupferschmidt DA, Lovinger DM (2014) Opioids induce dissociable forms of long-term depression of excitatory inputs to the dorsal striatum. Nat Neurosci 17:540–548. https://doi.org/10.1038/nn.3652
Bernstein H-G, Ortmann A, Dobrowolny H et al (2016) Bilaterally reduced claustral volumes in schizophrenia and major depressive disorder: a morphometric postmortem study. Eur Arch Psychiatry Clin Neurosci 266:25–33. https://doi.org/10.1007/s00406-015-0597-x
Braak H, Braak E (1982) Neuronal types in the claustrum of man. Anat Embryol (Berl) 163:447–460
Brand S (1981) A serial section Golgi analysis of the primate claustrum. Anat Embryol 162:475–488
Brumberg JC, Nowak LG, McCormick DA (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci 20:4829–4843
Callicott JH, Bertolino A, Mattay VS et al (2000) Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cereb Cortex 10:1078–1092. https://doi.org/10.1093/cercor/10.11.1078
Cho RY, Konecky RO, Carter CS (2006) Impairments in frontal cortical synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci 103:19878–19883. https://doi.org/10.1073/pnas.0609440103
Cozzi B, Roncon G, Granato A et al (2014) The claustrum of the bottlenose dolphin Tursiops truncatus (Montagu 1821). Front Syst Neurosci 8:42. https://doi.org/10.3389/fnsys.2014.00042
Crews FT, Boettiger CA (2009) Impulsivity, frontal lobes and risk for addiction. Pharmacol Biochem Behav 93:237–247. https://doi.org/10.1016/j.pbb.2009.04.018
Crick FC, Koch C (2005) What is the function of the claustrum? Philos Trans R Soc B Biol Sci 360:1271–1279. https://doi.org/10.1098/rstb.2005.1661
Dávila JC, Real M, Olmos L et al (2005) Embryonic and postnatal development of GABA, calbindin, calretinin, and parvalbumin in the mouse claustral complex. J Comp Neurol 481:42–57. https://doi.org/10.1002/cne.20347
Dinopoulos A, Papadopoulos GC, Michaloudi H et al (1992) Claustrum in the hedgehog (Erinaceus europaeus) brain: cytoarchitecture and connections with cortical and subcortical structures. J Comp Neurol 316:187–205. https://doi.org/10.1002/cne.903160205
Druckmann S, Banitt Y, Gidon A et al (2007) A novel multiple objective optimization framework for constraining conductance-based neuron models by experimental data. Front Neurosci 1:7–18. https://doi.org/10.3389/neuro.01.1.1.001.2007
Eiden LE, Mezey E, Eskay RL et al (1990) Neuropeptide content and connectivity of the rat claustrum. Brain Res 523:245–250
Ellender TJ, Huerta-Ocampo I, Deisseroth K et al (2011) Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine. J Neurosci 31:15340–15351. https://doi.org/10.1523/JNEUROSCI.3144-11.2011
Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652–669. https://doi.org/10.1038/nrn3119
Gu N, Vervaeke K, Storm JF (2007) BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J Physiol 580:859–882. https://doi.org/10.1113/jphysiol.2006.126367
Hinova-Palova DV, Edelstein L, Landzhov BV et al (2014) Parvalbumin-immunoreactive neurons in the human claustrum. Brain Struct Funct 219:1813–1830. https://doi.org/10.1007/s00429-013-0603-x
Hur EE, Zaborszky L (2005) Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization study [corrected]. J Comp Neurol 483:351–373. https://doi.org/10.1002/cne.20444
Kim U, McCormick DA (1998) The functional influence of burst and tonic firing mode on synaptic interactions in the thalamus. J Neurosci 18:9500–9516
Kim J, Matney CJ, Roth RH, Brown SP (2016) Synaptic organization of the neuronal circuits of the claustrum. J Neurosci 36:773–784. https://doi.org/10.1523/JNEUROSCI.3643-15.2016
Kong L, Bachmann S, Thomann PA et al (2012) Neurological soft signs and gray matter changes: a longitudinal analysis in first-episode schizophrenia. Schizophr Res 134:27–32. https://doi.org/10.1016/j.schres.2011.09.015
Kowiański P, Timmermans JP, Moryś J (2001) Differentiation in the immunocytochemical features of intrinsic and cortically projecting neurons in the rat claustrum—combined immunocytochemical and axonal transport study. Brain Res 905:63–71
Kowiański P, Moryś JM, Wójcik S et al (2003) Co-localisation of NOS with calcium-binding proteins during the postnatal development of the rat claustrum. Folia Morphol (Warsz) 62:211–214
Kowiański P, Moryś JM, Dziewiatkowski J et al (2008) NPY-, SOM- and VIP-containing interneurons in postnatal development of the rat claustrum. Brain Res Bull 76:565–571. https://doi.org/10.1016/j.brainresbull.2008.04.004
Kowiański P, Dziewiatkowski J, Moryś JM et al (2009) Colocalization of neuropeptides with calcium-binding proteins in the claustral interneurons during postnatal development of the rat. Brain Res Bull 80:100–106. https://doi.org/10.1016/j.brainresbull.2009.06.020
Kupferschmidt DA, Cody PA, Lovinger DM, Davis MI (2015) Brain BLAQ: post-hoc thick-section histochemistry for localizing optogenetic constructs in neurons and their distal terminals. Front Neuroanat 9:6. https://doi.org/10.3389/fnana.2015.00006
LeVay S, Sherk H (1981) The visual claustrum of the cat. I. Structure and connections. J Neurosci 1:956–980
Levin S (1984) Frontal lobe dysfunctions in schizophrenia—II. Impairments of psychological and brain functions. J Psychiatr Res 18:57–72. https://doi.org/10.1016/0022-3956(84)90047-5
Macosko EZ, Basu A, Satija R et al (2015) Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161:1202–1214. https://doi.org/10.1016/j.cell.2015.05.002
Madisen L, Zwingman TA, Sunkin SM et al (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133–140. https://doi.org/10.1038/nn.2467
Marvel CL, Paradiso S (2004) Cognitive and neurological impairment in mood disorders. Psychiatr Clin N Am 27:19–36. https://doi.org/10.1016/S0193-953X(03)00106-0
Mathur BN (2014) The claustrum in review. Front Syst Neurosci 8:48. https://doi.org/10.3389/fnsys.2014.00048
Mathur BN, Lovinger DM (2012) Endocannabinoid–dopamine interactions in striatal synaptic plasticity. Front Pharmacol 3:66. https://doi.org/10.3389/fphar.2012.00066
Mathur BN, Caprioli RM, Deutch AY (2009) Proteomic analysis illuminates a novel structural definition of the claustrum and insula. Cereb Cortex 19:2372–2379. https://doi.org/10.1093/cercor/bhn253
Mathur BN, Capik NA, Alvarez VA, Lovinger DM (2011) Serotonin induces long-term depression at corticostriatal synapses. J Neurosci 31:7402–7411. https://doi.org/10.1523/JNEUROSCI.6250-10.2011
Mathur BN, Tanahira C, Tamamaki N, Lovinger DM (2013) Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity. Nat Neurosci 16:1275–1283. https://doi.org/10.1038/nn.3478
Minzenberg MJ, Laird AR, Thelen S et al (2009) Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch Gen Psychiatry 66:811. https://doi.org/10.1001/archgenpsychiatry.2009.91
Morys J, Bobinski M, Wegiel J et al (1996) Alzheimer’s disease severely affects areas of the claustrum connected with the entorhinal cortex. J Hirnforsch 37:173–180
Patru MC, Reser DH (2015) A new perspective on delusional states—evidence for claustrum involvement. Front Psychiatry 6:158. https://doi.org/10.3389/fpsyt.2015.00158
Pirone A, Castagna M, Granato A et al (2014) Expression of calcium-binding proteins and selected neuropeptides in the human, chimpanzee, and crab-eating macaque claustrum. Front Syst Neurosci 8:99. https://doi.org/10.3389/fnsys.2014.00099
Pirone A, Magliaro C, Giannessi E, Ahluwalia A (2015) Parvalbumin expression in the claustrum of the adult dog. An immunohistochemical and topographical study with comparative notes on the structure of the nucleus. J Chem Neuroanat 64–65:33–42. https://doi.org/10.1016/j.jchemneu.2015.02.004
Rahman FE, Baizer JS (2007) Neurochemically defined cell types in the claustrum of the cat. Brain Res 1159:94–111. https://doi.org/10.1016/j.brainres.2007.05.011
Real MA, Dávila JC, Guirado S (2003) Expression of calcium-binding proteins in the mouse claustrum. J Chem Neuroanat 25:151–160
Reynhout K, Baizer JS (1999) Immunoreactivity for calcium-binding proteins in the claustrum of the monkey. Anat Embryol (Berl) 199:75–83
Smith JB, Alloway KD (2010) Functional specificity of claustrum connections in the rat: interhemispheric communication between specific parts of motor cortex. J Neurosci 30:16832–16844. https://doi.org/10.1523/JNEUROSCI.4438-10.2010
Sorensen SA, Bernard A, Menon V et al (2015) Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity. Cereb Cortex 25:433–449. https://doi.org/10.1093/cercor/bht243
Sugino K, Hempel CM, Miller MN et al (2006) Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 9:99–107. https://doi.org/10.1038/nn1618
Szalak R, Matysek M, Mozel S, Arciszewski MB (2015) Immunocytochemical detection of calretinin in the claustrum and endopiriform nucleus of the chinchilla. Pol J Vet Sci 18:857–863. https://doi.org/10.1515/pjvs-2015-0111
Tanahira C, Higo S, Watanabe K et al (2009) Parvalbumin neurons in the forebrain as revealed by parvalbumin-Cre transgenic mice. Neurosci Res 63:213–223. https://doi.org/10.1016/j.neures.2008.12.007
Wang Q, Ng L, Harris JA et al (2017) Organization of the connections between claustrum and cortex in the mouse. J Comp Neurol 525:1317–1346. https://doi.org/10.1002/cne.24047
Watakabe A, Hirokawa J, Ichinohe N et al (2012) Area-specific substratification of deep layer neurons in the rat cortex. J Comp Neurol 520:3553–3573. https://doi.org/10.1002/cne.23160
Watakabe A, Ohsawa S, Ichinohe N et al (2014) Characterization of claustral neurons by comparative gene expression profiling and dye-injection analyses. Front Syst Neurosci 8:98. https://doi.org/10.3389/fnsys.2014.00098
White MG, Mathur BN (2018) Frontal cortical control of posterior sensory and association cortices through the claustrum. Brain Struct Funct 223:1–8. https://doi.org/10.1007/s00429-018-1661-x
White MG, Cody PA, Bubser M et al (2017) Cortical hierarchy governs rat claustrocortical circuit organization. J Comp Neurol 525:1347–1362. https://doi.org/10.1002/cne.23970
White MG, Panicker M, Mu C et al (2018) Anterior cingulate cortex input to the claustrum is required for top-down action control. Cell Rep 22:84–95. https://doi.org/10.1016/j.celrep.2017.12.023
Williams SR, Stuart GJ (1999) Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol 521(Pt 2):467–482. https://doi.org/10.1111/J.1469-7793.1999.00467.X
Wójcik S, Dziewiatkowski J, Spodnik E et al (2004) Analysis of calcium binding protein immunoreactivity in the claustrum and the endopiriform nucleus of the rabbit. Acta Neurobiol Exp (Wars) 64:449–460
Yang CR, Seamans JK, Gorelova N (1996) Electrophysiological and morphological properties of layers V–VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neurosci 16:1904–1921
Acknowledgements
This work has been supported by National Institute on Alcohol Abuse and Alcoholism Grants K22AA021414 and R01AA024845 (B.N.M.), a Whitehall Foundation Grant 2014-12-68 (B.N.M.), National Institute of General Medical Sciences Grant T32GM008181 (M.G.W.), National Institute of Neurological Disorders and Stroke Grant T32NS063391 (M.G.W.), and National Institute of Mental Health Grant F31MH112350 (M.G.W.).
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MGW and BNM designed research, generated and analyzed data, and wrote the manuscript.
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White, M.G., Mathur, B.N. Claustrum circuit components for top–down input processing and cortical broadcast. Brain Struct Funct 223, 3945–3958 (2018). https://doi.org/10.1007/s00429-018-1731-0
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DOI: https://doi.org/10.1007/s00429-018-1731-0