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A direct anterior cingulate pathway to the primate primary olfactory cortex may control attention to olfaction

Abstract

Behavioral and functional studies in humans suggest that attention plays a key role in activating the primary olfactory cortex through an unknown circuit mechanism. We report that a novel pathway from the anterior cingulate cortex, an area which has a key role in attention, projects directly to the primary olfactory cortex in rhesus monkeys, innervating mostly the anterior olfactory nucleus. Axons from the anterior cingulate cortex formed synapses mostly with spines of putative excitatory pyramidal neurons and with a small proportion of a neurochemical class of inhibitory neurons that are thought to have disinhibitory effect on excitatory neurons. This novel pathway from the anterior cingulate is poised to exert a powerful excitatory effect on the anterior olfactory nucleus, which is a critical hub for odorant processing via extensive bilateral connections with primary olfactory cortices and the olfactory bulb. Acting on the anterior olfactory nucleus, the anterior cingulate may activate the entire primary olfactory cortex to mediate the process of rapid attention to olfactory stimuli.

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References

  1. Anderson JC, Binzegger T, Martin KA, Rockland KS (1998) The connection from cortical area V1 to V5: a light and electron microscopic study. J Neurosci 18(24):10525–10540

  2. Barbas H (1993) Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey. Neuroscience 56:841–864

  3. Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286(3):353–375. doi:10.1002/cne.902860306

  4. Botvinick MM (2007) Conflict monitoring and decision making: reconciling two perspectives on anterior cingulate function. Cogn Affect Behav Neurosci 7(4):356–366

  5. Bowman NE, Kording KP, Gottfried JA (2012) Temporal integration of olfactory perceptual evidence in human orbitofrontal cortex. Neuron 75(5):916–927. doi:10.1016/j.neuron.2012.06.035

  6. Boyett-Anderson JM, Lyons DM, Reiss AL, Schatzberg AF, Menon V (2003) Functional brain imaging of olfactory processing in monkeys. Neuroimage 20(1):257–264 pii:S105381190300288X

  7. Broca P (1879) Localisations Cérébrales: recherches sur les centres olfactifs. Rev D’anthropol 2(2):385–455

  8. Brunjes PC, Kenerson MC (2010) The anterior olfactory nucleus: quantitative study of dendritic morphology. J Comp Neurol 518(9):1603–1616. doi:10.1002/cne.22293

  9. Bunce JG, Barbas H (2011) Prefrontal pathways target excitatory and inhibitory systems in memory-related medial temporal cortices. Neuroimage 55(4):1461–1474. doi:10.1016/j.neuroimage.2011.01.064

  10. Cajal SR (1893) Estructura del asta de Ammon y fascia dentata. An Soc Esp Hist Nat 22

  11. Carmichael ST, Clugnet MC, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346(3):403–434. doi:10.1002/cne.903460306

  12. Carrapiso AI, Martin L, Jurado A, Garcia C (2010) Characterisation of the most odour-active compounds of bone tainted dry-cured Iberian ham. Meat Sci 85(1):54–58. doi:10.1016/j.meatsci.2009.12.003

  13. Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suarez F (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 10:220–242

  14. Cowan WM, Gottlieb DI, Hendrickson AE, Price JL, Woolsey TA (1972) The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res 37(1):21–51 pii:0006-8993(72)90344-7

  15. Crosby EC, Humphrey T (1939) Studies of the vertebrate telencephalon. I. The nuclear configuration of the olfactory and accessory olfactory formations and of the nucleus olfactorius anterior of certain reptiles, birds, and mammals. J Comp Neurol 71(1):121–213

  16. de Lorente Nó R (1934) Studies on the structure of the cerebral cortex. II. Continuation study of the ammonic system. J Psychol Neurol 46(2-3):113–177

  17. de Olmos J, Hardy H, Heimer L (1978) The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J Comp Neurol 181(2):213–244. doi:10.1002/cne.901810202

  18. DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28 K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14(1):1–19 pii:S0891061897100138

  19. DeFelipe J, Hendry SH, Jones EG (1989) Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res 503(1):49–54 pii:0006-8993(89)91702-2

  20. del Rio MR, DeFelipe J (1997) Synaptic connections of calretinin-immunoreactive neurons in the human neocortex. J Neurosci 17(13):5143–5154

  21. Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218(Pt 1):52–61. doi:10.1111/j.1365-2818.2005.01466.x

  22. Fiala JC, Harris KM (1999) Dendrite Structure. In: Stuart G, Spruston N, Häusser M (eds) Dendrites. Oxford University Press, Oxford, pp 1–34

  23. Fiala JC, Harris KM (2001a) Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc 8(1):1–16

  24. Fiala JC, Harris KM (2001b) Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J Microsc 202(Pt 3):468–472 pii:jmi926

  25. Franks KM, Russo MJ, Sosulski DL, Mulligan AA, Siegelbaum SA, Axel R (2011) Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 72(1):49–56. doi:10.1016/j.neuron.2011.08.020

  26. Fuster J (2008) Neuroimaging. In: Fuster J (ed) The prefrontal cortex. Academic Press, London, pp 285–331

  27. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y (2004) Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions. Neuroscience 125(3):615–623. doi:10.1016/j.neuroscience.2004.02.025

  28. Gavrilovici C, D’Alfonso S, Poulter MO (2010) Diverse interneuron populations have highly specific interconnectivity in the rat piriform cortex. J Comp Neurol 518(9):1570–1588. doi:10.1002/cne.22291

  29. Geinisman Y, Morrell F, de Toledo-Morrell L (1987) Axospinous synapses with segmented postsynaptic densities: a morphologically distinct synaptic subtype contributing to the number of profiles of ‘perforated’ synapses visualized in random sections. Brain Res 423(1–2):179–188 pii:0006-8993(87)90838-9

  30. Germuska M, Saha S, Fiala J, Barbas H (2006) Synaptic distinction of laminar-specific prefrontal-temporal pathways in primates. Cereb Cortex 16(6):865–875. doi:10.1093/cercor/bhj030

  31. Ghashghaei HT, Barbas H (2001) Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey. Neuroscience 103(3):593–614 pii:S0306452200005856

  32. Ghosh S, Larson SD, Hefzi H, Marnoy Z, Cutforth T, Dokka K, Baldwin KK (2011) Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472(7342):217–220. doi:10.1038/nature09945

  33. Gonchar Y, Burkhalter A (2003) Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J Neurosci 23(34):10904–10912 pii:23/34/10904

  34. Gottfried JA, Dolan RJ (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39(2):375–386

  35. Gottfried JA, Zelano C (2011) The value of identity: olfactory notes on orbitofrontal cortex function. Ann N Y Acad Sci 1239:138–148. doi:10.1111/j.1749-6632.2011.06268.x

  36. Greenough WT, West RW, DeVoogd TJ (1978) Subsynaptic plate perforations: changes with age and experience in the rat. Science 202(4372):1096–1098

  37. Gundersen HJ (1986) Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 143(Pt 1):3–45

  38. Haberly LB, Price JL (1977) The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res 129(1):152–157 pii:0006-8993(77)90978-7

  39. Haberly LB, Price JL (1978a) Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas. J Comp Neurol 178(4):711–740. doi:10.1002/cne.901780408

  40. Haberly LB, Price JL (1978b) Association and commissural fiber systems of the olfactory cortex of the rat. II. Systems originating in the olfactory peduncle. J Comp Neurol 181(4):781–807. doi:10.1002/cne.901810407

  41. Howard CV, Reed MG (1998) Unbiased Stereology, three-dimensional measurement in microscopy, vol 1. BIOS Scientific Publishers Limited, Oxford

  42. Howard JD, Plailly J, Grueschow M, Haynes JD, Gottfried JA (2009) Odor quality coding and categorization in human posterior piriform cortex. Nat Neurosci 12(7):932–938. doi:10.1038/nn.2324

  43. Illig KR, Eudy JD (2009) Contralateral projections of the rat anterior olfactory nucleus. J Comp Neurol 512(1):115–123. doi:10.1002/cne.21900

  44. Illig KR, Haberly LB (2003) Odor-evoked activity is spatially distributed in piriform cortex. J Comp Neurol 457(4):361–373. doi:10.1002/cne.10557

  45. Johnson DM, Illig KR, Behan M, Haberly LB (2000) New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that “primary” olfactory cortex functions like “association” cortex in other sensory systems. J Neurosci 20(18):6974–6982 pii:20/18/6974

  46. Kay RB, Brunjes PC (2011) Interneurons in the anterior olfactory nucleus/cortex. In: Society for Neuroscience Abstracts 2011, USA

  47. Kay LM, Freeman WJ (1998) Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behav Neurosci 112(3):541–553

  48. Kay RB, Meyer EA, Illig KR, Brunjes PC (2011) Spatial distribution of neural activity in the anterior olfactory nucleus evoked by odor and electrical stimulation. J Comp Neurol 519(2):277–289. doi:10.1002/cne.22519

  49. Kubota Y, Jones EG (1993) Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex. Brain Res 600(2):339–344 pii:0006-8993(93)91394-8

  50. Kubota Y, Hattori R, Yui Y (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649(1–2):159–173 pii:0006-8993(94)91060-X

  51. Lei H, Mooney R, Katz LC (2006) Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J Neurosci 26(46):12023–12032. doi:10.1523/JNEUROSCI.2598-06.2006

  52. Lord T, Kasprzak M (1989) Identification of self through olfaction. Percept Mot Skills 69(1):219–224

  53. Lundstrom JN, Boesveldt S, Albrecht J (2011) Central processing of the chemical senses: an overview. ACS Chem Neurosci 2(1):5–16. doi:10.1021/cn1000843

  54. Luskin MB, Price JL (1983a) The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216(3):264–291. doi:10.1002/cne.902160305

  55. Luskin MB, Price JL (1983b) The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol 216(3):292–302. doi:10.1002/cne.902160306

  56. McGinley MJ, Westbrook GL (2011) Membrane and synaptic properties of pyramidal neurons in the anterior olfactory nucleus. J Neurophysiol 105(4):1444–1453. doi:10.1152/jn.00715.2010

  57. Medalla M, Barbas H (2006) Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur J Neurosci 23(1):161–179. doi:10.1111/j.1460-9568.2005.04522.x

  58. Medalla M, Barbas H (2009) Synapses with inhibitory neurons differentiate anterior cingulate from dorsolateral prefrontal pathways associated with cognitive control. Neuron 61(4):609–620. doi:10.1016/j.neuron.2009.01.006

  59. Medalla M, Barbas H (2010) Anterior cingulate synapses in prefrontal areas 10 and 46 suggest differential influence in cognitive control. J Neurosci 30(48):16068–16081. doi:10.1523/JNEUROSCI.1773-10.2010

  60. Medalla M, Barbas H (2012) The anterior cingulate cortex may enhance inhibition of lateral prefrontal cortex via m2 cholinergic receptors at dual synaptic sites. J Neurosci 32(44):15611–15625. doi:10.1523/JNEUROSCI.2339-12.2012

  61. Medalla M, Lera P, Feinberg M, Barbas H (2007) Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in primates. Cereb Cortex 17(Suppl 1):i136–i150. doi:10.1093/cercor/bhm068

  62. Melchitzky DS, Sesack SR, Pucak ML, Lewis DA (1998) Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex. J Comp Neurol 390(2):211–224. doi:10.1002/(SICI)1096-9861(19980112)390:2<211:AID-CNE4>3.0.CO;2-4

  63. Melchitzky DS, Eggan SM, Lewis DA (2005) Synaptic targets of calretinin-containing axon terminals in macaque monkey prefrontal cortex. Neuroscience 130(1):185–195. doi:10.1016/j.neuroscience.2004.08.046

  64. Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379(1):113–132. doi:10.1002/(SICI)1096-9861(19970303)379:1<113:AID-CNE8>3.0.CO;2-7

  65. Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. III: efferent cortical output and comments on function. J Comp Neurol 212:38–52

  66. Meyer M, Allison AC (1949) An experimental investigation of the connexions of the olfactory tracts in the monkey. J Neurol Neurosurg Psychiatry 12(4):274–286 illust

  67. Meyer EA, Illig KR, Brunjes PC (2006) Differences in chemo- and cytoarchitectural features within pars principalis of the rat anterior olfactory nucleus suggest functional specialization. J Comp Neurol 498(6):786–795. doi:10.1002/cne.21077

  68. Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I, Wall NR, Taniguchi H, Tasic B, Huang ZJ, He Z, Callaway EM, Horowitz MA, Luo L (2011) Cortical representations of olfactory input by trans-synaptic tracing. Nature 472(7342):191–196 pii:nature0971410.1038/nature09714

  69. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87(4):675–686 pii:S0092-8674(00)81387-2

  70. Moore CT, Wilson CG, Mayer CA, Acquah SS, Massari VJ, Haxhiu MA (2004) A GABAergic inhibitory microcircuit controlling cholinergic outflow to the airways. J Appl Physiol 96(1):260–270. doi:10.1152/japplphysiol.00523.2003

  71. Mufson EJ, Mesulam MM (1982) Insula of the old world monkey. II. Afferent cortical input and comments on the claustrum. J Comp Neurol 212:23–37

  72. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18(4):599–612 pii:S0896-6273(00)80301-3

  73. Pessoa L (2008) On the relationship between emotion and cognition. Nat Rev Neurosci 9(2):148–158 pii:nrn231710.1038/nrn2317

  74. Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system. Neurons and their supporting cells. Oxford University Press, New York

  75. Pinto A, Jankowski M, Sesack SR (2003) Projections from the paraventricular nucleus of the thalamus to the rat prefrontal cortex and nucleus accumbens shell: ultrastructural characteristics and spatial relationships with dopamine afferents. J Comp Neurol 459(2):142–155. doi:10.1002/cne.10596

  76. Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, Kwong KK (2001) Activation and habituation in olfaction—an fMRI study. Neuroimage 13(4):547–560. doi:10.1006/nimg.2000.0713

  77. Poo C, Isaacson JS (2009) Odor representations in olfactory cortex: “sparse” coding, global inhibition, and oscillations. Neuron 62(6):850–861. doi:10.1016/j.neuron.2009.05.022

  78. Porter RH, Cernoch JM, McLaughlin FJ (1983) Maternal recognition of neonates through olfactory cues. Physiol Behav 30(1):151–154 pii:0031-9384(83)90051-3

  79. Price JL (1973) An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150(1):87–108. doi:10.1002/cne.901500105

  80. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG (2000) Pathway tracing using biotinylated dextran amines. J Neurosci Method 103(1):23–37 pii:S0165-0270(00)00293-4

  81. Rennaker RL, Chen CF, Ruyle AM, Sloan AM, Wilson DA (2007) Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J Neurosci 27(7):1534–1542. doi:10.1523/JNEUROSCI.4072-06.2007

  82. Ressler KJ, Sullivan SL, Buck LB (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79(7):1245–1255 pii:0092-8674(94)90015-9

  83. Reyher CK (1988) Persistence of the pars externa system of the anterior olfactory nucleus in a microsmatic primate, Callithrix jacchus. Brain Res 457(1):169–175 pii:0006-8993(88)90071-6

  84. Rihn LL, Claiborne BJ (1990) Dendritic growth and regression in rat dentate granule cells during late postnatal development. Brain Res Dev Brain Res 54(1):115–124

  85. Sasabe T, Kobayashi M, Kondo Y, Onoe H, Matsubara S, Yamamoto S, Tsukada H, Onoe K, Watabe H, Iida H, Kogo M, Sano K, Hatanaka A, Sawada T, Watanabe Y (2003) Activation of the anterior cingulate gyrus by ‘Green Odor’: a positron emission tomography study in the monkey. Chem Senses 28(7):565–572

  86. Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New York

  87. Sela L, Sobel N (2010) Human olfaction: a constant state of change-blindness. Exp Brain Res 205(1):13–29. doi:10.1007/s00221-010-2348-6

  88. Seubert J, Freiherr J, Djordjevic J, Lundstrom JN (2012) Statistical localization of human olfactory cortex. Neuroimage 66C:333–342. doi:10.1016/j.neuroimage.2012.10.030

  89. Shepherd GM (2007) Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad Sci 1121:87–101. doi:10.1196/annals.1401.032

  90. Siegmund B, Pollinger-Zierler B (2006) Odor thresholds of microbially induced off-flavor compounds in apple juice. J Agric Food Chem 54(16):5984–5989. doi:10.1021/jf060602n

  91. Simonyan K, Saad ZS, Loucks TM, Poletto CJ, Ludlow CL (2007) Functional neuroanatomy of human voluntary cough and sniff production. Neuroimage 37(2):401–409. doi:10.1016/j.neuroimage.2007.05.021

  92. Sirevaag AM, Greenough WT (1985) Differential rearing effects on rat visual cortex synapses. II. Synaptic morphometry. Brain Res 351(2):215–226

  93. Small DM, Prescott J (2005) Odor/taste integration and the perception of flavor. Exp Brain Res 166(3–4):345–357. doi:10.1007/s00221-005-2376-9

  94. Small DM, Voss J, Mak YE, Simmons KB, Parrish T, Gitelman D (2004) Experience-dependent neural integration of taste and smell in the human brain. J Neurophysiol 92(3):1892–1903. doi:10.1152/jn.00050.2004

  95. Small DM, Veldhuizen MG, Felsted J, Mak YE, McGlone F (2008) Separable substrates for anticipatory and consummatory food chemosensation. Neuron 57(5):786–797. doi:10.1016/j.neuron.2008.01.021

  96. Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392(6673):282–286. doi:10.1038/32654

  97. Sobel N, Prabhakaran V, Zhao Z, Desmond JE, Glover GH, Sullivan EV, Gabrieli JD (2000) Time course of odorant-induced activation in the human primary olfactory cortex. J Neurophysiol 83(1):537–551

  98. Sosulski DL, Bloom ML, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature 472(7342):213–216. doi:10.1038/nature09868

  99. Spence C, Kettenmann B, Kobal G, McGlone FP (2000) Selective attention to the chemosensory modality. Percept Psychophys 62(6):1265–1271

  100. Stettler DD, Axel R (2009) Representations of odor in the piriform cortex. Neuron 63(6):854–864. doi:10.1016/j.neuron.2009.09.005

  101. Stevens CF (2003) Neurotransmitter release at central synapses. Neuron 40(2):381–388 pii:S0896627303006433

  102. Suzuki N, Bekkers JM (2010) Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comp Neurol 518(10):1670–1687. doi:10.1002/cne.22295

  103. Tabert MH, Steffener J, Albers MW, Kern DW, Michael M, Tang H, Brown TR, Devanand DP (2007) Validation and optimization of statistical approaches for modeling odorant-induced fMRI signal changes in olfactory-related brain areas. Neuroimage 34(4):1375–1390. doi:10.1016/j.neuroimage.2006.11.020

  104. Turner W (1890) The convolutions of the brain: a study in comparative anatomy. J Anat Physiol 25(Pt 1):105–153

  105. Turner BH, Gupta KC, Mishkin M (1978) The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta. J Comp Neurol 177(3):381–396. doi:10.1002/cne.901770303

  106. Valverde F (1965) Studies on the piriform lobe. Harvard University Press, Cambridge

  107. Valverde F, Lopez-Mascaraque L, De Carlos JA (1989) Structure of the nucleus olfactorius anterior of the hedgehog (Erinaceus europaeus). J Comp Neurol 279(4):581–600. doi:10.1002/cne.902790407

  108. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79(6):981–991 pii:0092-8674(94)90029-9

  109. Veenman CL, Reiner A, Honig MG (1992) Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J Neurosci Method 41(3):239–254

  110. Veldhuizen MG, Small DM (2011) Modality-specific neural effects of selective attention to taste and odor. Chem Sens 36(8):747–760. doi:10.1093/chemse/bjr043

  111. Whisman ML (1978) Odorant evaluation: a study of ethanediol and tetrahydrothiophene as warning agents in propane. Environ Sci Technol 12(12):1285–1288

  112. Widen H, Leufven A, Nielsen T (2005) Identification of chemicals, possibly originating from misuse of refillable PET bottles, responsible for consumer complaints about off-odours in water and soft drinks. Food Addit Contam 22(7):681–692. doi:10.1080/02652030500159987

  113. Yan Z, Tan J, Qin C, Lu Y, Ding C, Luo M (2008) Precise circuitry links bilaterally symmetric olfactory maps. Neuron 58(4):613–624. doi:10.1016/j.neuron.2008.03.012

  114. Zald DH, Pardo JV (2000) Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol 36(2):165–181 pii:S0167-8760(99)00110-5

  115. Zelano C, Bensafi M, Porter J, Mainland J, Johnson B, Bremner E, Telles C, Khan R, Sobel N (2005) Attentional modulation in human primary olfactory cortex. Nat Neurosci 8(1):114–120. doi:10.1038/nn1368

  116. Zelano C, Montag J, Khan R, Sobel N (2009) A specialized odor memory buffer in primary olfactory cortex. PLoS One 4(3):e4965. doi:10.1371/journal.pone.0004965

  117. Zelano C, Mohanty A, Gottfried JA (2011) Olfactory predictive codes and stimulus templates in piriform cortex. Neuron 72(1):178–187. doi:10.1016/j.neuron.2011.08.010

  118. Zikopoulos B, Barbas H (2006) Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J Neurosci 26(28):7348–7361. doi:10.1523/JNEUROSCI.5511-05.2006

  119. Zikopoulos B, Barbas H (2007) Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLoS One 2(9):e848. doi:10.1371/journal.pone.0000848

  120. Zikopoulos B, Barbas H (2012) Pathways for emotions and attention converge on the thalamic reticular nucleus in primates. J Neurosci 32(15):5338–5350. doi:10.1523/JNEUROSCI.4793-11.2012

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Acknowledgments

We thank Isabel Park and Justin Tepes for technical assistance; Marcia Feinberg and Clare Timbie for outstanding electron microscopy assistance; Dr. Ron Killiany for assistance with imaging; Dr. Angela Carville and Dr. Leah Makaron for veterinary care and surgical assistance; Dr. Basilis Zikopoulos, Dr. Jamie Bunce, Dr. Yohan John and Dr. Maria Medalla for helpful discussion of the manuscript. This work was supported by National Institutes of Health grants from the National Institute of Neurological Disorders and Stroke (R01NS024760) and the National Institute of Mental Health (RO1MH057414); and by Center of Excellence for Learning in Education, Science and Technology (CELEST), a National Science Foundation Science of Learning Center (NSF SBE-0354378). M. Á. García-Cabezas was the recipient in 2010 of a Short Stay Grant from Fundación Alicia Koplowitz (Spain).

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The authors declare that they have no conflict of interest.

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Correspondence to Helen Barbas.

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García-Cabezas, M.Á., Barbas, H. A direct anterior cingulate pathway to the primate primary olfactory cortex may control attention to olfaction. Brain Struct Funct 219, 1735–1754 (2014). https://doi.org/10.1007/s00429-013-0598-3

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Keywords

  • Olfaction
  • Attention
  • Anterior cingulate cortex
  • Primary olfactory cortex
  • Anterior olfactory nucleus
  • Posterior orbitofrontal cortex