Thalamic neuromodulation and its implications for executive networks

Frontiers in Neural Circuits

Volumn 8, Issue JUNE, 2014, Pages

  Varela, Carmen ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Acetylcholine; Dopamine; Histamine; Intralaminar; Midline; Modulators; Noradrenaline; Serotonin

Indexed keywords

ACETYLCHOLINE; DOPAMINE; HISTAMINE; NORADRENALIN; OREXIN; SEROTONIN; MIDLINE;

BASAL GANGLION; CHOLINERGIC SYSTEM; COGNITION; CORPUS STRIATUM; DENDRITE; DEPOLARIZATION; DOPAMINERGIC SYSTEM; EXECUTIVE FUNCTION; GABAERGIC SYSTEM; HUMAN; HYPERPOLARIZATION; LATERAL GENICULATE BODY; MEDIAL PREFRONTAL CORTEX; NERVE POTENTIAL; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; NORADRENERGIC SYSTEM; PARAVENTRICULAR THALAMIC NUCLEUS; PREFRONTAL CORTEX; REVIEW; SEROTONINERGIC SYSTEM; SYNAPSE; THALAMUS; THALAMUS INTRALAMINAR NUCLEUS; THALAMUS MIDLINE NUCLEUS; ANIMAL; ATTENTION; INTRALAMINAR; MODULATORS; NERVE CELL NETWORK; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ACETYLCHOLINE; DOPAMINE; HISTAMINE; INTRALAMINAR; MIDLINE; MODULATORS; NORADRENALINE; SEROTONIN;

ANIMALS; ATTENTION; EXECUTIVE FUNCTION; NERVE NET; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 84907198628     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00069     Document Type: Review

References (240)

1. Abramson, B. P., and Chalupa, L. M. (1985). The laminar distribution of cortical connections with the tecto-and cortico-recipient zones in the cat's lateral posterior nucleus. Neuroscience 15, 81-95. doi: 10.1016/0306-4522(85)90125-3
2. Albrecht, D., Quäschling, U., Zippel, U., and Davidowa, H. (1996). Effects of dopamine on neurons of the lateral geniculate nucleus: an iontophoretic study. Synapse 23, 70-78. doi: 10.1002/(SICI)1098-2396(199606)23:2<70::AID-SYN2>3.0.CO;2-D
3. Alexander, G. M., Fisher, T. L., and Godwin, D. W. (2006). Differential response dynamics of corticothalamic glutamatergic synapses in the lateral geniculate nucleus and thalamic reticular nucleus. Neuroscience 137, 367-372. doi: 10.1016/j.neuroscience.2005.11.012
4. Alexander, G. M., and Godwin, D. W. (2005). Presynaptic inhibition of corticothalamic feedback by metabotropic glutamate receptors. J. Neurophysiol. 94, 163-175. doi: 10.1152/jn.01198.2004
5. Alloway, K. D., Olson, M. L., and Smith, J. B. (2008). Contralateral corticothalamic projections from MI whisker cortex: potential route for modulating hemispheric interactions. J. Comp. Neurol. 510, 100-116. doi: 10.1002/cne.21782
6. Alsene, K. M., Rajbhandari, A. K., Ramaker, M. J., and Bakshi, V. P. (2011). Discrete forebrain neuronal networks supporting noradrenergic regulation of sensorimotor gating. Neuropsychopharmacology 36, 1003-1014. doi: 10.1038/npp.2010.238
7. Baldauf, Z. B., Wang, S., Chomsung, R. D., May, P. J., and Bickford, M. E. (2005). Ultrastructural analysis of projections to the pulvinar nucleus of the cat. II: Pretectum. J. Comp. Neurol. 485, 108-126. doi: 10.1002/cne.20487
8. Bartlett, E. L., Stark, J. M., Guillery, R. W., and Smith, P. H. (2000). Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience 100, 811-828. doi: 10.1016/S0306-4522(00)00340-7
9. Bayer, L., Eggermann, E., Saint-Mleux, B., Machard, D., Jones, B. E., Mühlethaler, M., et al. (2002). Selective action of orexin (hypocretin) on nonspecific thalamocortical projection neurons. J. Neurosci. 22, 7835-7839.
10. Beatty, J. A., Sylwestrak, E. L., and Cox, C. L. (2009). Two distinct populations of projection neurons in the rat lateral parafascicular thalamic nucleus and their cholinergic responsiveness. Neuroscience 162, 155-173. doi: 10.1016/j.neuroscience.2009.04.043
11. Bender, D. B., and Youakim, M. (2001). Effect of attentive fixation in macaque thalamus and cortex. J. Neurophysiol. 85, 219-234.
12. Bickford, M. E., Günlük, A. E., Guido, W., and Sherman, S. M. (1993). Evidence that cholinergic axons from the parabrachial region of the brainstem are the exclusive source of nitric oxide in the lateral geniculate nucleus of the cat. J. Comp. Neurol. 334, 410-430. doi: 10.1002/cne.903340307
13. Bickford, M. E., Ramcharan, E., Godwin, D. W., Erisir, A., Gnadt, J., and Sherman, S. M. (2000). Neurotransmitters contained in the subcortical extraretinal inputs to the monkey lateral geniculate nucleus. J. Comp. Neurol. 424, 701-717. doi: 10.1002/1096-9861(20000904)424:4<701::AID-CNE11>3.0.CO;2-B
14. Billet, S., Cant, N. B., and Hall, W. C. (1999). Cholinergic projections to the visual thalamus and superior colliculus. Brain Res. 847, 121-123. doi: 10.1016/S0006-8993(99)01900-9
15. Blandina, P., Munari, L., Provensi, G., and Passani, M. B. (2012). Histamine neurons in the tuberomamillary nucleus: a whole center or distinct subpopulations? Front. Syst. Neurosci. 6:33. doi: 10.3389/fnsys.2012.00033
16. Block, A. E., Dhanji, H., Thompson-Tardif, S. F., and Floresco, S. B. (2007). Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb. Cortex 17, 1625-1636. doi: 10.1093/cercor/bhl073
17. Bolton, R. F., Cornwall, J., and Phillipson, O. T. (1993). Collateral axons of cholinergic pontine neurones projecting to midline, mediodorsal and parafascicular thalamic nuclei in the rat. J. Chem. Neuroanat. 6, 101-114. doi: 10.1016/0891-0618(93)90031-X
18. Bourassa, J., and Deschênes, M. (1995). Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 66, 253-263. doi: 10.1016/0306-4522(95)00009-8
19. Bourassa, J., Pinault, D., and Deschênes, M. (1995). Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur. J. Neurosci. 7, 19-30. doi: 10.1111/j.1460-9568.1995.tb01016.x
20. Briggs, F. (2010). Organizing principles of cortical layer 6. Front. Neural Circuits 4:3. doi: 10.3389/neuro.04.003.2010
21. Briggs, F., and Usrey, W. M. (2011). Corticogeniculate feedback and visual processing in the primate. J. Physiol. (Lond.) 589, 33-40. doi: 10.1113/jphysiol.2010.193599
22. Brown, H. D., Baker, P. M., and Ragozzino, M. E. (2010). The parafascicular thalamic nucleus concomitantly influences behavioral flexibility and dorsomedial striatal acetylcholine output in rats. J. Neurosci. 30, 14390-14398. doi: 10.1523/JNEUROSCI.2167-10.2010
23. Buzsaki, G., Bickford, R. G., Ponomareff, G., Thal, L. J., Mandel, R., and Gage, F. H. (1988). Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8, 4007-4026.
24. Byrum, C. E., and Guyenet, P. G. (1987). Afferent and efferent connections of the A5 noradrenergic cell group in the rat. J. Comp. Neurol. 261, 529-542. doi: 10.1002/cne.902610406
25. Cappe, C., Morel, A., and Rouiller, E. M. (2007). Thalamocortical and the dual pattern of corticothalamic projections of the posterior parietal cortex in macaque monkeys. Neuroscience 146, 1371-1387. doi: 10.1016/j.neuroscience.2007.02.033
26. Cassel, J.-C., Pereira de Vasconcelos, A., Loureiro, M., Cholvin, T., Dalrymple-Alford, J. C., and Vertes, R. P. (2013). The reuniens and rhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog. Neurobiol. 111, 34-52. doi: 10.1016/j.pneurobio.2013.08.006
27. Cenquizca, L. A., and Swanson, L. W. (2006). An analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat. J. Comp. Neurol. 497, 101-114. doi: 10.1002/cne.20985
28. Chapin, E. M., and Andrade, R. (2001a). A 5-HT(7) receptor-mediated depolarization in the anterodorsal thalamus. I. Pharmacological characterization. J. Pharmacol. Exp. Ther. 297, 395-402.
29. Chapin, E. M., and Andrade, R. (2001b). A 5-HT(7) receptor-mediated depolarization in the anterodorsal thalamus. II. Involvement of the hyperpolarization-activated current I(h). J. Pharmacol. Exp. Ther. 297, 403-409.
30. Choi, D. L., Davis, J. F., Magrisso, I. J., Fitzgerald, M. E., Lipton, J. W., and Benoit, S. C. (2012). Orexin signaling in the paraventricular thalamic nucleus modulates mesolimbic dopamine and hedonic feeding in the rat. Neuroscience 210, 243-248. doi: 10.1016/j.neuroscience.2012.02.036
31. Cholvin, T., Loureiro, M., Cassel, R., Cosquer, B., Geiger, K., De Sa Nogueira, D., et al. (2013). The ventral midline thalamus contributes to strategy shifting in a memory task requiring both prefrontal cortical and hippocampal functions. J. Neurosci. 33, 8772-8783. doi: 10.1523/JNEUROSCI.0771-13.2013
32. Clascá, F., Rubio-Garrido, P., and Jabaudon, D. (2012). Unveiling the diversity of thalamocortical neuron subtypes. Eur. J. Neurosci. 35, 1524-1532. doi: 10.1111/j.1460-9568.2012.08033.x
33. Conley, M., and Raczkowski, D. (1990). Sublaminar organization within layer VI of the striate cortex in Galago. J. Comp. Neurol. 302, 425-436. doi: 10.1002/cne.903020218
34. Cornwall, J., and Phillipson, O. T. (1988). Afferent projections to the dorsal thalamus of the rat as shown by retrograde lectin transport. II. The midline nuclei. Brain Res. Bull. 21, 147-161. doi: 10.1016/0361-9230(88)90227-4
35. Crandall, S. R., and Cox, C. L. (2013). Thalamic microcircuits: presynaptic dendrites form two feedforward inhibitory pathways in thalamus. J. Neurophysiol. 110, 470-480. doi: 10.1152/jn.00559.2012
36. Cropper, E. C., Eisenman, J. S., and Azmitia, E. C. (1984). An immunocytochemical study of the serotonergic innervation of the thalamus of the rat. J. Comp. Neurol. 224, 38-50. doi: 10.1002/cne.902240104
37. Cucchiaro, J. B., Uhlrich, D. J., and Sherman, S. M. (1988). Parabrachial innervation of the cat's dorsal lateral geniculate nucleus: an electron microscopic study using the tracer Phaseolus vulgaris leucoagglutinin (PHA-L). J. Neurosci. 8, 4576-4588.
38. Cudeiro, J., and Sillito, A. M. (2006). Looking back: corticothalamic feedback and early visual processing. Trends Neurosci. 29, 298-306. doi: 10.1016/j.tins.2006.05.002
39. Curró Dossi, R., Paré, D., and Steriade, M. (1991). Short-lasting nicotinic and long-lasting muscarinic depolarizing responses of thalamocortical neurons to stimulation of mesopontine cholinergic nuclei. J. Neurophysiol. 65, 393-406.
40. Davoodi, F. G., Motamedi, F., Akbari, E., Ghanbarian, E., and Jila, B. (2011). Effect of reversible inactivation of reuniens nucleus on memory processing in passive avoidance task. Behav. Brain Res. 221, 1-6. doi: 10.1016/j.bbr.2011.02.020
41. De Lima, A. D., and Singer, W. (1987). The brainstem projection to the lateral geniculate nucleus in the cat: identification of cholinergic and monoaminergic elements. J. Comp. Neurol. 259, 92-121. doi: 10.1002/cne.902590107
42. Dekker, J. J., and Kuypers, H. G. (1976). Quantitative EM study of projection terminal in the rats AV thalamic nucleus. Autoradiographic and degeneration techniques compared. Brain Res. 117, 399-422. doi: 10.1016/0006-8993(76)90750-2
43. Destexhe, A., Neubig, M., Ulrich, D., and Huguenard, J. (1998). Dendritic low-threshold calcium currents in thalamic relay cells. J. Neurosci. 18, 3574-3588.
44. Devilbiss, D. M., and Waterhouse, B. D. (2011). Phasic and tonic patterns of locus coeruleus output differentially modulate sensory network function in the awake rat. J. Neurophysiol. 105, 69-87. doi: 10.1152/jn.00445.2010
45. Ding, J. B., Guzman, J. N., Peterson, J. D., Goldberg, J. A., and Surmeier, D. J. (2010). Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67, 294-307. doi: 10.1016/j.neuron.2010.06.017
46. Dolleman-van der Weel, M. J., Morris, R. G. M., and Witter, M. P. (2009). Neurotoxic lesions of the thalamic reuniens or mediodorsal nucleus in rats affect non-mnemonic aspects of watermaze learning. Brain Struct. Funct.213, 329-342. doi: 10.1007/s00429-008-0200-6
47. Ellender, T. J., Huerta-Ocampo, I., Deisseroth, K., Capogna, M., and Bolam, J. P. (2011). Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine. J. Neurosci. 31, 15340-15351. doi: 10.1523/JNEUROSCI.3144-11.2011
48. Erisir, A., Van Horn, S. C., Bickford, M. E., and Sherman, S. M. (1997a). Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: a comparison with corticogeniculate terminals. J. Comp. Neurol. 377, 535-549. doi: 10.1002/(SICI)1096-9861(19970127)377:4<535::AID-CNE5>3.0.CO;2-3
49. Erisir, A., Van Horn, S. C., and Sherman, S. M. (1997b). Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc. Natl. Acad. Sci. U.S.A. 94, 1517-1520. doi: 10.1073/pnas.94.4.1517
50. Favero, M., Varghese, G., and Castro-Alamancos, M. A. (2012). The state of somatosensory cortex during neuromodulation. J. Neurophysiol. 108, 1010-1024. doi: 10.1152/jn.00256.2012
51. Fitzpatrick, D., Conley, M., Luppino, G., Matelli, M., and Diamond, I. T. (1988). Cholinergic projections from the midbrain reticular formation and the parabigeminal nucleus to the lateral geniculate nucleus in the tree shrew. J. Comp. Neurol. 272, 43-67. doi: 10.1002/cne.902720105
52. Fitzpatrick, D., Diamond, I. T., and Raczkowski, D. (1989). Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J. Comp. Neurol. 288, 647-675. doi: 10.1002/cne.902880411
53. Floresco, S. B., and Magyar, O. (2006). Mesocortical dopamine modulation of executive functions: beyond working memory. Psychopharmacology (Berl.) 188, 567-585. doi: 10.1007/s00213-006-0404-5
54. Francesconi, W., Müller, C. M., and Singer, W. (1988). Cholinergic mechanisms in the reticular control of transmission in the cat lateral geniculate nucleus. J. Neurophysiol. 59, 1690-1718.
55. Fuller, P. M., Sherman, D., Pedersen, N. P., Saper, C. B., and Lu, J. (2011). Reassessment of the structural basis of the ascending arousal system. J. Comp. Neurol. 519, 933-956. doi: 10.1002/cne.22559
56. Galvan, A., and Smith, Y. (2011). The primate thalamostriatal systems: anatomical organization, functional roles and possible involvement in Parkinson's disease. Basal Ganglia 1, 179-189. doi: 10.1016/j.baga.2011.09.001
57. García-Cabezas, M. A., Martínez-Sánchez, P., Sánchez-González, M. A., Garzón, M., and Cavada, C. (2009). Dopamine innervation in the thalamus: monkey versus rat. Cereb. Cortex 19, 424-434. doi: 10.1093/cercor/bhn093
58. Giguere, M., and Goldman-Rakic, P. S. (1988). Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J. Comp. Neurol. 277, 195-213. doi: 10.1002/cne.902770204
59. Goaillard, J.-M., and Vincent, P. (2002). Serotonin suppresses the slow afterhyperpolarization in rat intralaminar and midline thalamic neurones by activating 5-HT(7) receptors. J. Physiol. (Lond.) 541, 453-465. doi: 10.1113/jphysiol.2001.013896
60. Godwin, D. W., Van Horn, S. C., Eriir, A., Sesma, M., Romano, C., and Sherman, S. M. (1996). Ultrastructural localization suggests that retinal and cortical inputs access different metabotropic glutamate receptors in the lateral geniculate nucleus. J. Neurosci. 16, 8181-8192.
61. Gonzalo-Ruiz, A., Lieberman, A. R., and Sanz-Anquela, J. M. (1995). Organization of serotoninergic projections from the raphé nuclei to the anterior thalamic nuclei in the rat: a combined retrograde tracing and 5-HT immunohistochemical study. J. Chem. Neuroanat. 8, 103-115. doi: 10.1016/0891-0618(94)00039-V
62. Govindaiah, G., and Cox, C. L. (2005). Excitatory actions of dopamine via D1-like receptors in the rat lateral geniculate nucleus. J. Neurophysiol. 94, 3708-3718. doi: 10.1152/jn.00583.2005
63. Govindaiah, G., Wang, T., Gillette, M. U., Crandall, S. R., and Cox, C. L. (2010). Regulation of inhibitory synapses by presynaptic D4 dopamine receptors in thalamus. J. Neurophysiol. 104, 2757-2765. doi: 10.1152/jn.00361.2010
64. Grasso, C., Li Volsi, G., Licata, F., Ciranna, L., and Santangelo, F. (2006). Aminergic control of neuronal firing rate in thalamic motor nuclei of the rat. Arch. Ital. Biol. 144, 173-196.
65. Gritti, I., Mariotti, M., and Mancia M. (1998). GABAergic and cholinergic basal forebrain and preoptic-anterior hypothalamic projections to the mediodorsal nucleus of the thalamus in the cat. Neuroscience 85, 149-178. doi: 10.1016/S0306-4522(97)00573-3
66. Groenewegen, H. J. (1988). Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24, 379-431. doi: 10.1016/0306-4522(88)90339-9
67. Guillery, R. W. (1995). Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J. Anat. 187(Pt 3), 583-592.
68. Guillery, R. W., and Sherman, S. M. (2002). Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33, 163-175. doi: 10.1016/S0896-6273(01)00582-7
69. Gutierrez, C., Cox, C. L., Rinzel, J., and Sherman, S. M. (2001). Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus. J. Neurosci. 21, 1022-1032.
70. Hallanger, A. E., Levey, A. I., Lee, H. J., Rye, D. B., and Wainer, B. H. (1987). The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. Comp. Neurol. 262, 105-124. doi: 10.1002/cne.902620109.
71. Hallanger, A. E., Price, S. D., Lee, H. J., Steininger, T. L., and Wainer, B. H. (1990). Ultrastructure of cholinergic synaptic terminals in the thalamic anteroventral, ventroposterior, and dorsal lateral geniculate nuclei of the rat. J. Comp. Neurol. 299, 482-492. doi: 10.1002/cne.902990408
72. Hallock, H. L., Wang, A., Shaw, C. L., and Griffin, A. L. (2013). Transient inactivation of the thalamic nucleus reuniens and rhomboid nucleus produces deficits of a working-memory dependent tactile-visual conditional discrimination task. Behav. Neurosci. 127, 860-866. doi: 10.1037/a0034653
73. Hazama, M., Kimura, A., Donishi, T., Sakoda, T., and Tamai, Y. (2004). Topography of corticothalamic projections from the auditory cortex of the rat. Neuroscience 124, 655-667. doi: 10.1016/j.neuroscience.2003.12.027
74. Heckers, S., Geula, C., and Mesulam, M. M. (1992). Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J. Comp. Neurol. 325, 68-82. doi: 10.1002/cne.903250107
75. Hembrook, J. R., and Mair, R. G. (2011). Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win-shift performance. Hippocampus 21, 815-826. doi: 10.1002/hipo.20797
76. Hobson, J. A., Stickgold, R., and Pace-Schott, E. F. (1998). The neuropsychology of REM sleep dreaming. Neuroreport 9, R1-R14. doi: 10.1097/00001756-199802160-00033
77. Hoover, W. B., and Vertes, R. P. (2007). Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct. 212, 149-179. doi: 10.1007/s00429-007-0150-4
78. Hu, B., Steriade, M., and Deschênes, M. (1989). The effects of brainstem peribrachial stimulation on perigeniculate neurons: the blockage of spindle waves. Neuroscience 31, 1-12. doi: 10.1016/0306-4522(89)90026-2
79. Hughes, H. C., and Mullikin, W. H. (1984). Brainstem afferents to the lateral geniculate nucleus of the cat. Exp. Brain Res. 54, 253-258. doi: 10.1007/BF00236224
80. Igelstrom, K. M., Herbison, A. E., and Hyland, B. I. (2010). Enhanced c-Fos expression in superior colliculus, paraventricular thalamus and septum during learning of cue-reward association. Neuroscience 168, 706-714. doi: 10.1016/j.neuroscience.2010.04.018
81. Jacobson, S., and Trojanowski, J. Q. (1975). Corticothalamic neurons and thalamocortical terminal fields: an investigation in rat using horseradish peroxidase and autoradiography. Brain Res. 85, 385-401. doi: 10.1016/0006-8993(75)90815-X
82. Jahnsen, H., and Llinás, R. (1984). Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. (Lond.) 349, 205-226.
83. Jones, E. G. (2007). The Thalamus 1. Cambridge: Cambridge University Press.
84. Jones, H. E., Andolina, I. M., Ahmed, B., Shipp, S. D., Clements, J. T. C., Grieve, K. L., et al. (2012). Differential feedback modulation of center and surround mechanisms in parvocellular cells in the visual thalamus. J. Neurosci.32, 15946-15951. doi: 10.1523/JNEUROSCI.0831-12.2012
85. Jurgens, C. W. D., Bell, K. A., McQuiston, A. R., and Guido, W. (2012). Optogenetic stimulation of the corticothalamic pathway affects relay cells and GABAergic neurons differently in the mouse visual thalamus. PLoS ONE 7:e45717. doi: 10.1371/journal.pone.0045717
86. Kaitz, S. S., and Robertson, R. T. (1981). Thalamic connections with limbic cortex. II. Corticothalamic projections. J. Comp. Neurol. 195, 527-545. doi: 10.1002/cne.901950309
87. Kakei, S., Na, J., and Shinoda, Y. (2001). Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J. Comp. Neurol. 437, 170-185. doi: 10.1002/cne.1277
88. Kato, S., Kuramochi, M., Kobayashi, K., Fukabori, R., Okada, K., Uchigashima, M., et al. (2011). Selective neural pathway targeting reveals key roles of thalamostriatal projection in the control of visual discrimination. J. Neurosci. 31, 17169-17179. doi: 10.1523/JNEUROSCI.4005-11.2011
89. Kawai, H., Lazar, R., and Metherate, R. (2007). Nicotinic control of axon excitability regulates thalamocortical transmission. Nat. Neurosci. 10, 1168-1175. doi: 10.1038/nn1956
90. Kayama, Y., Shimada, S., Hishikawa, Y., and Ogawa, T. (1989). Effects of stimulating the dorsal raphe nucleus of the rat on neuronal activity in the dorsal lateral geniculate nucleus. Brain Res. 489, 1-11. doi: 10.1016/0006-8993(89)90002-4
91. Kelley, A. E., Baldo, B. A., and Pratt, W. E. (2005). A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J. Comp. Neurol. 493, 72-85. doi: 10.1002/cne.20769
92. Kelly, J. P., and Wong, D. (1981). Laminar connections of the cat's auditory cortex. Brain Res. 212, 1-15. doi: 10.1016/0006-8993(81)90027-5
93. Kha, H. T., Finkelstein, D. I., Pow, D. V., Lawrence, A. J., and Horne, M. K. (2000). Study of projections from the entopeduncular nucleus to the thalamus of the rat. J. Comp. Neurol. 426, 366-377. doi: 10.1002/1096-9861(20001023)426:3<366::AID-CNE2>3.0.CO;2-B
94. Kha, H. T., Finkelstein, D. I., Tomas, D., Drago, J., Pow, D. V., and Horne, M. K. (2001). Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: single axon reconstructions and immunohistochemical study. J. Comp. Neurol. 440, 20-30. doi: 10.1002/cne.1367
95. Killackey, H. P., and Sherman, S. M. (2003). Corticothalamic projections from the rat primary somatosensory cortex. J. Neurosci. 23, 7381-7384.
96. Kirifides, M. L., Simpson, K. L., Lin, R. C., and Waterhouse, B. D. (2001). Topographic organization and neurochemical identity of dorsal raphe neurons that project to the trigeminal somatosensory pathway in the rat. J. Comp. Neurol. 435, 325-340. doi: 10.1002/cne.1033
97. Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., et al. (2014). Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346. doi: 10.1038/nmeth.2836
98. Krubitzer, L. A., and Seelke, A. M. H. (2012). Cortical evolution in mammals: the bane and beauty of phenotypic variability. Proc. Natl. Acad. Sci. U.S.A. 109(Suppl. 1), 10647-10654. doi: 10.1073/pnas.1201891109
99. Kultas-Ilinsky, K., and Ilinsky, I. A. (1991). Fine structure of the ventral lateral nucleus (VL) of the Macaca mulattathalamus: cell types and synaptology. J. Comp. Neurol. 314, 319-349. doi: 10.1002/cne.903140209
100. Kupfer, D. J., Frank, E., and Phillips, M. L. (2012). Major depressive disorder: new clinical, neurobiological, and treatment perspectives. Lancet 379, 1045-1055. doi: 10.1016/S0140-6736(11)60602-8
101. Kuroda, M., Murakami, K., Igarashi, H., and Okada, A. (1996). The convergence of axon terminals from the mediodorsal thalamic nucleus and ventral tegmental area on pyramidal cells in layer V of the rat prelimbic cortex. Eur. J. Neurosci. 8, 1340-1349. doi: 10.1111/j.1460-9568.1996.tb01596.x
102. Kuroda, M., and Price, J. L. (1991). Ultrastructure and synaptic organization of axon terminals from brainstem structures to the mediodorsal thalamic nucleus of the rat. J. Comp. Neurol. 313, 539-552. doi: 10.1002/cne.903130313
103. Kusnoor, S. V., Bubser, M., and Deutch, A. Y. (2012). The effects of nigrostriatal dopamine depletion on the thalamic parafascicular nucleus. Brain Res. 1446, 46-55. doi: 10.1016/j.brainres.2012.01.040
104. Lam, Y.-W., and Sherman, S. M. (2010). Functional organization of the somatosensory cortical layer 6 feedback to the thalamus. Cereb. Cortex 20, 13-24. doi: 10.1093/cercor/bhp077
105. Landisman, C. E., and Connors, B. W. (2007). VPM and PoM nuclei of the rat somatosensory thalamus: intrinsic neuronal properties and corticothalamic feedback. Cereb. Cortex 17, 2853-2865. doi: 10.1093/cercor/bhm025
106. Lavin, A., and Grace, A. A. (1998). Dopamine modulates the responsivity of mediodorsal thalamic cells recorded in vitro. J. Neurosci. 18, 10566-10578.
107. Lavoie, B., and Parent, A. (1991). Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J. Comp. Neurol. 312, 1-18. doi: 10.1002/cne.903120102
108. Lee, H. J., Rye, D. B., Hallanger, A. E., Levey, A. I., and Wainer, B. H. (1988). Cholinergic vs. noncholinergic efferents from the mesopontine tegmentum to the extrapyramidal motor system nuclei. J. Comp. Neurol. 275, 469-492. doi: 10.1002/cne.902750402
109. Lee, S., Carvell, G. E., and Simons, D. J. (2008). Motor modulation of afferent somatosensory circuits. Nat. Neurosci. 11, 1430-1438. doi: 10.1038/nn.2227
110. Lee, S.-H., and Dan, Y. (2012). Neuromodulation of brain states. Neuron 76, 209-222. doi: 10.1016/j.neuron.2012.09.012
111. Lesch, K.-P., and Waider, J. (2012). Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 76, 175-191. doi: 10.1016/j.neuron.2012.09.013
112. Lévesque, M., and Parent, A. (1998). Axonal arborization of corticostriatal and corticothalamic fibers arising from prelimbic cortex in the rat. Cereb. Cortex 8, 602-613. doi: 10.1093/cercor/8.7.602
113. Levey, A. I., Hallanger, A. E., and Wainer, B. H. (1987). Choline acetyltransferase immunoreactivity in the rat thalamus. J. Comp. Neurol. 257, 317-332. doi: 10.1002/cne.902570302
114. Lisman, J. (2012). Excitation, inhibition, local oscillations, or large-scale loops: what causes the symptoms of schizophrenia? Curr. Opin. Neurobiol. 22, 537-544. doi: 10.1016/j.conb.2011.10.018
115. Liu, X. B., Honda, C. N., and Jones, E. G. (1995). Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J. Comp. Neurol. 352, 69-91. doi: 10.1002/cne.903520106
116. Liu, X. B., and Jones, E. G. (1991). The fine structure of serotonin and tyrosine hydroxylase immunoreactive terminals in the ventral posterior thalamic nucleus of cat and monkey. Exp. Brain Res. 85, 507-518. doi: 10.1007/BF00231734
117. Llinás, R., Ribary, U., Contreras, D., and Pedroarena, C. (1998). The neuronal basis for consciousness. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1841-1849. doi: 10.1098/rstb.1998.0336
118. Llinás, R. R., Ribary, U., Jeanmonod, D., Kronberg, E., and Mitra, P. P. (1999). Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc. Natl. Acad. Sci. U.S.A. 96, 15222-15227. doi: 10.1073/pnas.96.26.15222
119. Losier, B. J., and Semba, K. (1993). Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res. 604, 41-52. doi: 10.1016/0006-8993(93)90350-V
120. Lyons, M. K. (2011). Deep brain stimulation: current and future clinical applications. Mayo Clin. Proc. 86, 662-672. doi: 10.4065/mcp.2011.0045
121. MacLeod, N. K., James, T. A., and Starr, M. S. (1984). Muscarinic action of acetylcholine in the rat ventromedial thalamic nucleus. Exp. Brain Res. 55, 553-561. doi: 10.1007/BF00235286
122. Manning, K. A., Wilson, J. R., and Uhlrich, D. J. (1996). Histamine-immunoreactive neurons and their innervation of visual regions in the cortex, tectum, and thalamus in the primate Macaca mulatta. J. Comp. Neurol. 373, 271-282. doi: 10.1002/(SICI)1096-9861(19960916)373:2<271::AID-CNE9>3.0.CO;2-0
123. Marks, G. A., and Roffwarg, H. P. (1989). The cholinergic influence upon rat dorsal lateral geniculate nucleus is dependent on state of arousal. Brain Res. 494, 294-306. doi: 10.1016/0006-8993(89)90598-2
124. Martin-Fardon, R., and Boutrel, B. (2012). Orexin/hypocretin (Orx/Hcrt) transmission and drug-seeking behavior: is the paraventricular nucleus of the thalamus (PVT) part of the drug seeking circuitry? Front. Behav. Neurosci. 6:75. doi: 10.3389/fnbeh.2012.00075
125. Masterson, S. P., Li, J., and Bickford, M. E. (2009). Synaptic organization of the tectorecipient zone of the rat lateral posterior nucleus. J. Comp. Neurol. 515, 647-663. doi: 10.1002/cne.22077
126. Matsumoto, N., Minamimoto, T., Graybiel, A. M., and Kimura, M. (2001). Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol. 85, 960-976.
127. Maunsell, J. H. R., and Cook, E. P. (2002). The role of attention in visual processing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 1063-1072. doi: 10.1098/rstb.2002.1107
128. McCormick, D. A. (1992). Cellular mechanisms underlying cholinergic and noradrenergic modulation of neuronal firing mode in the cat and guinea pig dorsal lateral geniculate nucleus. J. Neurosci. 12, 278-289.
129. McCormick, D. A., and Pape, H. C. (1988). Acetylcholine inhibits identified interneurons in the cat lateral geniculate nucleus. Nature 334, 246-248. doi: 10.1038/334246a0
130. McCormick, D. A., and Pape, H. C. (1990). Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. J. Physiol. (Lond.) 431, 319-342.
131. McCormick, D. A., and Prince, D. A. (1986). Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature 319, 402-405. doi: 10.1038/319402a0
132. McCormick, D. A., and Prince, D. A. (1987). Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei, in vitro. J. Physiol. (Lond.) 392, 147-165.
133. McCormick, D. A., and Prince, D. A. (1988). Noradrenergic modulation of firing pattern in guinea pig and cat thalamic neurons, in vitro. J. Neurophysiol. 59, 978-996.
134. McCormick, D. A., and von Krosigk, M. (1992). Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. Proc. Natl. Acad. Sci. U.S.A. 89, 2774-2778. doi: 10.1073/pnas.89.7.2774
135. McCormick, D. A., and Williamson, A. (1991). Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: possible cellular mechanisms of histaminergic control of arousal. J. Neurosci. 11, 3188-3199.
136. McKenna, J. T., and Vertes, R. P. (2004). Afferent projections to nucleus reuniens of the thalamus. J. Comp. Neurol.480, 115-142. doi: 10.1002/cne.20342
137. Melchitzky, D. S., Erickson, S. L., and Lewis, D. A. (2006). Dopamine innervation of the monkey mediodorsal thalamus: location of projection neurons and ultrastructural characteristics of axon terminals. Neuroscience 143, 1021-1030. doi: 10.1016/j.neuroscience.2006.08.056
138. Mesulam, M. M., Mufson, E. J., Wainer, B. H., and Levey, A. I. (1983). Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10, 1185-1201. doi: 10.1016/0306-4522(83)90108-2
139. Miyata, M., and Imoto, K. (2006). Different composition of glutamate receptors in corticothalamic and lemniscal synaptic responses and their roles in the firing responses of ventrobasal thalamic neurons in juvenile mice. J. Physiol. 575, 161-174. doi: 10.1113/jphysiol.2006.114413
140. Mize, R. R., and Payne, M. P. (1987). The innervation density of serotonergic (5-HT) fibers varies in different subdivisions of the cat lateral geniculate nucleus complex. Neurosci. Lett. 82, 133-139. doi: 10.1016/0304-3940(87)90117-0
141. Molinari, M., Minciacchi, D., Bentivoglio, M., and Macchi, G. (1985). Efferent fibers from the motor cortex terminate bilaterally in the thalamus of rats and cats. Exp. Brain Res. 57, 305-312. doi: 10.1007/BF00236536
142. Monckton, J. E., and McCormick, D. A. (2002). Neuromodulatory role of serotonin in the ferret thalamus. J. Neurophysiol. 87, 2124-2136. doi: 10.1152/jn.00650.2001
143. Monti, J. M. (2011). Serotonin control of sleep-wake behavior. Sleep Med. Rev. 15, 269-281. doi: 10.1016/j.smrv.2010.11.003
144. Mooney, D. M., Zhang, L., Basile, C., Senatorov, V. V., Ngsee, J., Omar, A., et al. (2004). Distinct forms of cholinergic modulation in parallel thalamic sensory pathways. Proc. Natl. Acad. Sci. U.S.A. 101, 320-324. doi: 10.1073/pnas.0304445101
145. Morrison, J. H., and Foote, S. L. (1986). Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. J. Comp. Neurol. 243, 117-138. doi: 10.1002/cne.902430110
146. Moruzzi, G., and Magoun, H. W. (1949). Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455-473. doi: 10.1016/0013-4694(49)90219-9
147. Moxon, K. A., Devilbiss, D. M., Chapin, J. K., and Waterhouse, B. D. (2007). Influence of norepinephrine on somatosensory neuronal responses in the rat thalamus: a combined modeling and in vivo multi-channel, multi-neuron recording study. Brain Res. 1147, 105-123. doi: 10.1016/j.brainres.2007.02.006
148. Murphy, P. C., Duckett, S. G., and Sillito, A. M. (1999). Feedback connections to the lateral geniculate nucleus and cortical response properties. Science 286, 1552-1554. doi: 10.1126/science.286.5444.1552
149. Murphy, P. C., Duckett, S. G., and Sillito, A. M. (2000). Comparison of the laminar distribution of input from areas 17 and 18 of the visual cortex to the lateral geniculate nucleus of the cat. J. Neurosci. 20, 845-853.
150. Murphy, P. C., Uhlrich, D. J., Tamamaki, N., and Sherman, S. M. (1994). Brain-stem modulation of the response properties of cells in the cat's perigeniculate nucleus. Vis. Neurosci. 11, 781-791. doi: 10.1017/S0952523800003084
151. Négyessy, L., Hámori, J., and Bentivoglio, M. (1998). Contralateral cortical projection to the mediodorsal thalamic nucleus: origin and synaptic organization in the rat. Neuroscience 84, 741-753. doi: 10.1016/S0306-4522(97)00559-9
152. Niswender, C. M., and Conn, P. J. (2010). Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 50, 295-322. doi: 10.1146/annurev.pharmtox.011008.145533
153. Nothias, F., Onteniente, B., Roudier, F., and Peschanksi, M. (1988). Immunocytochemical study of serotoninergic and noradrenergic innervation of the ventrobasal complex of the rat thalamus. Neurosci. Lett. 95, 59-63. doi: 10.1016/0304-3940(88)90632-5
154. Ojima, H. (1994). Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb. Cortex 4, 646-663. doi: 10.1093/cercor/4.6.646
155. Olsen, S. R., Bortone, D. S., Adesnik, H., and Scanziani, M. (2012). Gain control by layer six in cortical circuits of vision. Nature 483, 47-52. doi: 10.1038/nature10835
156. Pais-Vieira, M., Lebedev, M. A., Wiest, M. C., and Nicolelis, M. A. L. (2013). Simultaneous top-down modulation of the primary somatosensory cortex and thalamic nuclei during active tactile discrimination. J. Neurosci. 33, 4076-4093. doi: 10.1523/JNEUROSCI.1659-12.2013
157. Pape, H. C., and McCormick, D. A. (1989). Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 340, 715-718. doi: 10.1038/340715a0
158. Paré, D., Smith, Y., Parent, A., and Steriade, M. (1988). Projections of brainstem core cholinergic and non-cholinergic neurons of cat to intralaminar and reticular thalamic nuclei. Neuroscience 25, 69-86. doi: 10.1016/0306-4522(88)90007-3
159. Parent, A., Paré, D., Smith, Y., and Steriade, M. (1988). Basal forebrain cholinergic and noncholinergic projections to the thalamus and brainstem in cats and monkeys. J. Comp. Neurol. 277, 281-301. doi: 10.1002/cne.902770209
160. Parent, M., and Descarries, L. (2008). Acetylcholine innervation of the adult rat thalamus: distribution and ultrastructural features in dorsolateral geniculate, parafascicular, and reticular thalamic nuclei. J. Comp. Neurol.511, 678-691. doi: 10.1002/cne.21868
161. Pasik, P., Pasik, T., and Holstein, G. R. (1988). Serotonin-immunoreactivity in the monkey lateral geniculate nucleus. Exp. Brain Res. 69, 662-666. doi: 10.1007/BF00247318
162. Paxinos, G., and Watson, C. (2004). The Rat Brain in Stereotaxic Coordinates-The New Coronal Set, 5th Edn. San Diego, CA: Academic Press.
163. Petrof, I., Viaene, A. N., and Sherman, S. M. (2012). Two populations of corticothalamic and interareal corticocortical cells in the subgranular layers of the mouse primary sensory cortices. J. Comp. Neurol. 520, 1678-1686. doi: 10.1002/cne.23006
164. Picciotto, M. R., Higley, M. J., and Mineur, Y. S. (2012). Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76, 116-129. doi: 10.1016/j.neuron.2012.08.036
165. Pifl, C., Hornykiewicz, O., Blesa, J., Adánez, R., Cavada, C., and Obeso, J. A. (2013). Reduced noradrenaline, but not dopamine and serotonin in motor thalamus of the MPTP primate: relation to severity of parkinsonism. J. Neurochem. 125, 657-662. doi: 10.1111/jnc.12162
166. Piggott, M. A., Ballard, C. G., Dickinson, H. O., McKeith, I. G., Perry, R. H., and Perry, E. K. (2007). Thalamic D2 receptors in dementia with Lewy bodies, Parkinson's disease, and Parkinson's disease dementia. Int. J. Neuropsychopharmacol. 10, 231-244. doi: 10.1017/S146114570600647X
167. Pinto, A., Jankowski, M., and Sesack, S. R. (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, 142-155. doi: 10.1002/cne.10596
168. Prasad, J. A., Macgregor, E. M., and Chudasama, Y. (2013). Lesions of the thalamic reuniens cause impulsive but not compulsive responses. Brain Struct. Funct. 218, 85-96. doi: 10.1007/s00429-012-0378-5
169. Price, J. L., and Slotnick, B. M. (1983). Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study. J. Comp. Neurol. 215, 63-77. doi: 10.1002/cne.902150106
170. Purvis, C. C., and Duncan, M. J. (1997). Discrete thalamic lesions attenuate winter adaptations and increase body weight. Am. J. Physiol. 273, R226-R235.
171. Raczkowski, D., Hamos, J. E., and Sherman, S. M. (1988). Synaptic circuitry of physiologically identified W-cells in the cat's dorsal lateral geniculate nucleus. J. Neurosci. 8, 31-48.
172. Ramcharan, E. J., Gnadt, J. W., and Sherman, S. M. (2005). Higher-order thalamic relays burst more than first-order relays. Proc. Natl. Acad. Sci. U.S.A. 102, 12236-12241. doi: 10.1073/pnas.0502843102
173. Reichova, I., and Sherman, S. M. (2004). Somatosensory corticothalamic projections: distinguishing drivers from modulators. J. Neurophysiol. 92, 2185-2197. doi: 10.1152/jn.00322.2004
174. Rieck, R. W., Ansari, M. S., Whetsell, W. O. Jr., Deutch, A. Y., and Kessler, R. M. (2004). Distribution of dopamine D2-like receptors in the human thalamus: autoradiographic and PET studies. Neuropsychopharmacology 29, 362-372. doi: 10.1038/sj.npp.1300336
175. Risold, P. Y., Thompson, R. H., and Swanson, L. W. (1997). The structural organization of connections between hypothalamus and cerebral cortex. Brain Res. Brain Res. Rev. 24, 197-254. doi: 10.1016/S0165-0173(97)00007-6
176. Rivadulla, C., Martínez, L. M., Varela, C., and Cudeiro, J. (2002). Completing the corticofugal loop: a visual role for the corticogeniculate type 1 metabotropic glutamate receptor. J. Neurosci. 22, 2956-2962.
177. Robson, J. A. (1983). The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat. J. Comp. Neurol. 216, 89-103. doi: 10.1002/cne.902160108
178. Rockland, K. S. (1996). Two types of corticopulvinar terminations: round (type 2) and elongate (type 1). J. Comp. Neurol. 368, 57-87. doi: 10.1002/(SICI)1096-9861(19960422)368:1<57::AID-CNE5>3.0.CO;2-J
179. Saalmann, Y. B., Pinsk, M. A., Wang, L., Li, X., and Kastner, S. (2012). The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337, 753-756. doi: 10.1126/science.1223082
180. Sakurai, T. (2007). The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat. Rev. Neurosci. 8, 171-181. doi: 10.1038/nrn2092
181. Salt, T. E., and Turner, J. P. (1998). Modulation of sensory inhibition in the ventrobasal thalamus via activation of group II metabotropic glutamate receptors by 2R,4R-aminopyrrolidine-2,4-dicarboxylate. Exp. Brain Res. 121, 181-185. doi: 10.1007/s002210050450
182. Sánchez-González, M. A., García-Cabezas, M. A., Rico, B., and Cavada, C. (2005). The primate thalamus is a key target for brain dopamine. J. Neurosci. 25, 6076-6083. doi: 10.1523/JNEUROSCI.0968-05.2005
183. Saper, C. B. (1984). Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J. Comp. Neurol. 222, 313-342. doi: 10.1002/cne.902220302
184. Saper, C. B., and Loewy, A. D. (1980). Efferent connections of the parabrachial nucleus in the rat. Brain Res. 197, 291-317. doi: 10.1016/0006-8993(80)91117-8
185. Scharfman, H. E., Lu, S. M., Guido, W., Adams, P. R., and Sherman, S. M. (1990). N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proc. Natl. Acad. Sci. U.S.A. 87, 4548-4552. doi: 10.1073/pnas.87.12.4548
186. Schiff, N. D., Giacino, J. T., Kalmar, K., Victor, J. D., Baker, K., Gerber, M., et al. (2007). Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603. doi: 10.1038/nature06041
187. Semba, K., Reiner, P. B., and Fibiger, H. C. (1990). Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 38, 643-654. doi: 10.1016/0306-4522(90)90058-C
188. Sherman, S. M. (2001). Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122-126. doi: 10.1016/S0166-2236(00)01714-8
189. Sherman, S. M., and Guillery, R. W. (1998). On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators. " Proc. Natl. Acad. Sci. U.S.A. 95, 7121-7126. doi: 10.1073/pnas.95.12.7121
190. Shiromani, P. J., Floyd, C., and Velázquez-Moctezuma, J. (1990). Pontine cholinergic neurons simultaneously innervate two thalamic targets. Brain Res. 532, 317-322. doi: 10.1016/0006-8993(90)91774-B
191. Sillito, A. M., Cudeiro, J., and Jones, H. E. (2006). Always returning: feedback and sensory processing in visual cortex and thalamus. Trends Neurosci. 29, 307-316. doi: 10.1016/j.tins.2006.05.001
192. Sillito, A. M., Kemp, J. A., and Berardi, N. (1983). The cholinergic influence on the function of the cat dorsal lateral geniculate nucleus (dLGN). Brain Res. 280, 299-307. doi: 10.1016/0006-8993(83)90059-8
193. Simpson, K. L., Altman, D. W., Wang, L., Kirifides, M. L., Lin, R. C., and Waterhouse, B. D. (1997). Lateralization and functional organization of the locus coeruleus projection to the trigeminal somatosensory pathway in rat. J. Comp. Neurol. 385, 135-147. doi: 10.1002/(SICI)1096-9861(19970818)385:1<135::AID-CNE8>3.0.CO;2-3
194. Simpson, K. L., Waterhouse, B. D., and Lin, R. C. (1999). Origin, distribution, and morphology of galaninergic fibers in the rodent trigeminal system. J. Comp. Neurol. 411, 524-534. doi: 10.1002/(SICI)1096-9861(19990830)411:3<524::AID-CNE13>3.0.CO;2-X
195. Simpson, K. L., Waterhouse, B. D., and Lin, R. C. S. (2003). Differential expression of nitric oxide in serotonergic projection neurons: neurochemical identification of dorsal raphe inputs to rodent trigeminal somatosensory targets. J. Comp. Neurol. 466, 495-512. doi: 10.1002/cne.10912
196. Sittig, N., and Davidowa, H. (2001). Histamine reduces firing and bursting of anterior and intralaminar thalamic neurons and activates striatal cells in anesthetized rats. Behav. Brain Res. 124, 137-143. doi: 10.1016/S0166-4328(01)00223-6
197. Smith, Y., Bennett, B. D., Bolam, J. P., Parent, A., and Sadikot, A. F. (1994). Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J. Comp. Neurol. 344, 1-19. doi: 10.1002/cne.903440102
198. Smith, Y., Paré, D., Deschênes, M., Parent, A., and Steriade, M. (1988). Cholinergic and non-cholinergic projections from the upper brainstem core to the visual thalamus in the cat. Exp. Brain Res. 70, 166-180.
199. Smith, Y., Raju, D., Nanda, B., Pare, J. F., Galvan, A., and Wichmann, T. (2009). The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states. Brain Res. Bull. 78, 60-68. doi: 10.1016/j.brainresbull.2008.08.015
200. Sofroniew, M. V., Priestley, J. V., Consolazione, A., Eckenstein, F., and Cuello, A. C. (1985). Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res. 329, 213-223. doi: 10.1016/0006-8993(85)90527-X
201. Spreafico, R., Amadeo, A., Angoscini, P., Panzica, F., and Battaglia, G. (1993). Branching projections from mesopontine nuclei to the nucleus reticularis and related thalamic nuclei: a double labelling study in the rat. J. Comp. Neurol. 336, 481-492. doi: 10.1002/cne.903360402
202. Steriade, M., Paré, D., Parent, A., and Smith, Y. (1988). Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey. Neuroscience 25, 47-67. doi: 10.1016/0306-4522(88)90006-1
203. Strakhova, M. I., Nikkel, A. L., Manelli, A. M., Hsieh, G. C., Esbenshade, T. A., Brioni, J. D., et al. (2009). Localization of histamine H4 receptors in the central nervous system of human and rat. Brain Res. 1250, 41-48. doi: 10.1016/j.brainres.2008.11.018
204. Sun, Y.-G., and Beierlein, M. (2011). Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses. J. Neurophysiol. 105, 2319-2329. doi: 10.1152/jn.00942.2010
205. Swanson, L. W., and Hartman, B. K. (1975). The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J. Comp. Neurol. 163, 467-505. doi: 10.1002/cne.901630406
206. Takahashi, K., Lin, J.-S., and Sakai, K. (2006). Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse. J. Neurosci. 26, 10292-10298. doi: 10.1523/JNEUROSCI.2341-06.2006
207. Temereanca, S., and Simons, D. J. (2004). Functional topography of corticothalamic feedback enhances thalamic spatial response tuning in the somatosensory whisker/barrel system. Neuron 41, 639-651. doi: 10.1016/S0896-6273(04)00046-7
208. Theyel, B. B., Llano, D. A., and Sherman, S. M. (2010). The corticothalamocortical circuit drives higher-order cortex in the mouse. Nat. Neurosci. 13, 84-88. doi: 10.1038/nn.2449
209. Thomson, A. M. (2010). Neocortical layer 6, a review. Front. Neuroanat. 4:13. doi: 10.3389/fnana.2010.00013
210. Turner, J. P., and Salt, T. E. (1999). Group III metabotropic glutamate receptors control corticothalamic synaptic transmission in the rat thalamus in vitro. J. Physiol. (Lond.) 519(Pt 2), 481-491. doi: 10.1111/j.1469-7793.1999.0481m.x
211. Turner, J. P., and Salt, T. E. (2000). Synaptic activation of the group I metabotropic glutamate receptor mGlu1 on the thalamocortical neurons of the rat dorsal lateral geniculate nucleus in vitro. Neuroscience 100, 493-505. doi: 10.1016/S0306-4522(00)00280-3
212. Turner, J. P., and Salt, T. E. (2003). Group II and III metabotropic glutamate receptors and the control of the nucleus reticularis thalami input to rat thalamocortical neurones in vitro. Neuroscience 122, 459-469. doi: 10.1016/j.neuroscience.2003.08.014
213. Ueda, S., and Sano, Y. (1986). Distributional pattern of serotonin-immunoreactive nerve fibers in the lateral geniculate nucleus of the rat, cat and monkey (Macaca fuscata). Cell Tissue Res. 243, 249-253. doi: 10.1007/BF00251038
214. Uhlrich, D. J., Cucchiaro, J. B., and Sherman, S. M. (1988). The projection of individual axons from the parabrachial region of the brain stem to the dorsal lateral geniculate nucleus in the cat. J. Neurosci. 8, 4565-4575.
215. Uhlrich, D. J., Manning, K. A., and Pienkowski, T. P. (1993). The histaminergic innervation of the lateral geniculate complex in the cat. Vis. Neurosci. 10, 225-235. doi: 10.1017/S0952523800003631
216. Uhlrich, D. J., Manning, K. A., and Xue, J.-T. (2002). Effects of activation of the histaminergic tuberomammillary nucleus on visual responses of neurons in the dorsal lateral geniculate nucleus. J. Neurosci. 22, 1098-1107.
217. Van Horn, S. C., and Sherman, S. M. (2007). Fewer driver synapses in higher order than in first order thalamic relays. Neuroscience 146, 463-470. doi: 10.1016/j.neuroscience.2007.01.026
218. Varela, C. (2013). The gating of neocortical information by modulators. J. Neurophysiol. 109, 1229-1232. doi: 10.1152/jn.00701.2012
219. Varela, C., and Sherman, S. M. (2007). Differences in response to muscarinic activation between first and higher order thalamic relays. J. Neurophysiol. 98, 3538-3547. doi: 10.1152/jn.00578.2007
220. Varela, C., and Sherman, S. M. (2009). Differences in response to serotonergic activation between first and higher order thalamic nuclei. Cereb. Cortex 19, 1776-1786. doi: 10.1093/cercor/bhn208
221. Varela, C., Kumar, S., Yang, J. Y., and Wilson, M. A. (2014). Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens. Brain Struct. Funct. 219, 911-929. doi: 10.1007/s00429-013-0543-5
222. Vertes, R. P. (1991). A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J. Comp. Neurol. 313, 643-668. doi: 10.1002/cne.903130409
223. Vertes, R. P., Fortin, W. J., and Crane, A. M. (1999). Projections of the median raphe nucleus in the rat. J. Comp. Neurol. 407, 555-582. doi: 10.1002/(SICI)1096-9861(19990517)407:4<555::AID-CNE7>3.0.CO;2-E
224. Vertes, R. P., Linley, S. B., Groenewegen, H. J., and Witter, M. P. (2014). "Thalamus, " in The Rat Nervous System, 4th Edn, ed. G. Paxinos (San Diego, CA: Academic Press).
225. Vertes, R. P., Linley, S. B., and Hoover, W. B. (2010). Pattern of distribution of serotonergic fibers to the thalamus of the rat. Brain Struct. Funct. 215, 1-28. doi: 10.1007/s00429-010-0249-x
226. Viaene, A. N., Petrof, I., and Sherman, S. M. (2013). Activation requirements for metabotropic glutamate receptors. Neurosci. Lett. 541, 67-72. doi: 10.1016/j.neulet.2013.02.004
227. Vincent, S. R., Staines, W. A., McGeer, E. G., and Fibiger, H. C. (1980). Transmitters contained in the efferents of the habenula. Brain Res. 195, 479-484. doi: 10.1016/0006-8993(80)90084-0
228. Vogt, B. A., Hof, P. R., Friedman, D. P., Sikes, R. W., and Vogt, L. J. (2008). Norepinephrinergic afferents and cytology of the macaque monkey midline, mediodorsal, and intralaminar thalamic nuclei. Brain Struct. Funct. 212, 465-479. doi: 10.1007/s00429-008-0178-0
229. Wang, B., Gonzalo-Ruiz, A., Morte, L., Campbell, G., and Lieberman, A. R. (1999). Immunoelectron microscopic study of glutamate inputs from the retrosplenial granular cortex to identified thalamocortical projection neurons in the anterior thalamus of the rat. Brain Res. Bull. 50, 63-76. doi: 10.1016/S0361-9230(99)00092-1
230. Wang, W., Jones, H. E., Andolina, I. M., Salt, T. E., and Sillito, A. M. (2006). Functional alignment of feedback effects from visual cortex to thalamus. Nat. Neurosci. 9, 1330-1336. doi: 10.1038/nn1768
231. Williams, S. R., and Stuart, G. J. (2000). Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J. Neurosci. 20, 1307-1317.
232. Wilson, J. R., Friedlander, M. J., and Sherman, S. M. (1984). Fine structural morphology of identified X-and Y-cells in the cat's lateral geniculate nucleus. Proc. R. Soc. Lond. B Biol. Sci. 221, 411-436. doi: 10.1098/rspb.1984.0042
233. Wilson, J. R., Manning, K. A., Forestner, D. M., Counts, S. E., and Uhlrich, D. J. (1999). Comparison of cholinergic and histaminergic axons in the lateral geniculate complex of the macaque monkey. Anat. Rec. 255, 295-305. doi: 10.1002/(SICI)1097-0185(19990701)255:3<295::AID-AR5>3.0.CO;2-Q
234. Woolf, N. J., and Butcher, L. L. (1986). Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res. Bull. 16, 603-637. doi: 10.1016/0361-9230(86)90134-6
235. Xu, W., and Südhof, T. C. (2013). A neural circuit for memory specificity and generalization. Science 339, 1290-1295. doi: 10.1126/science.1229534
236. Zhao, Y., Kerscher, N., Eysel, U., and Funke, K. (2001). Changes of contrast gain in cat dorsal lateral geniculate nucleus by dopamine receptor agonists. Neuroreport 12, 2939-2945. doi: 10.1097/00001756-200109170-00037
237. Zhao, Y., Kerscher, N., Eysel, U., and Funke, K. (2002). D1 and D2 receptor-mediated dopaminergic modulation of visual responses in cat dorsal lateral geniculate nucleus. J. Physiol. (Lond.) 539, 223-238. doi: 10.1113/jphysiol.2001.012721
238. Zhu, J., and Heggelund, P. (2001). Muscarinic regulation of dendritic and axonal outputs of rat thalamic interneurons: a new cellular mechanism for uncoupling distal dendrites. J. Neurosci. 21, 1148-1159.
239. Zhu, J. J., and Uhlrich, D. J. (1997). Nicotinic receptor-mediated responses in relay cells and interneurons in the rat lateral geniculate nucleus. Neuroscience 80, 191-202. doi: 10.1016/S0306-4522(97)00095-X
240. Zhu, J. J., and Uhlrich, D. J. (1998). Cellular mechanisms underlying two muscarinic receptor-mediated depolarizing responses in relay cells of the rat lateral geniculate nucleus. Neuroscience 87, 767-781. doi: 10.1016/S0306-4522(98)00209-7