Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition

Frontiers in Systems Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Saalmann, Yuri B ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Anesthesia; Attention; Mediodorsal nucleus; Memory; Neural synchrony; Reuniens nucleus; Reward; Schizophrenia

Indexed keywords

ANTERIOR INTRALAMINAR NUCLEUS; AROUSAL; ATTENTION; BRAIN CELL; BRAIN FUNCTION; COGNITION; COMMUNICATION THEORY; CONSCIOUSNESS; CORTICAL SYNCHRONIZATION; HIPPOCAMPUS; HUMAN; MEMORY; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; ORIENTING REFLEX; PHYSIOLOGY; POSTERIOR INTRALAMINAR NUCLEUS; PREFRONTAL CORTEX; PULVINAR; REVIEW; TEMPORAL LOBE; THALAMUS DORSOMEDIAL NUCLEUS; THALAMUS INTRALAMINAR NUCLEUS; THALAMUS MEDIAL NUCLEUS; THALAMUS MIDLINE NUCLEUS; THALAMUS NUCLEUS; THALAMUS POSTERIOR NUCLEUS;

EID: 84900564392     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00083     Document Type: Review

References (88)

1. Aertsen, A. M., Gerstein, G. L., Habib, M. K., and Palm, G. (1989). Dynamics of neuronal firing correlation: modulation of "effective connectivity". J. Neuro-physiol. 61, 900-917.
2. Akert, K., and Hartmann-Von Monakow, K. (1980). Relationships of precentral premotor and prefrontal cortex to the mediodorsal and intralaminar nuclei of the monkey thalamus. Acta Neurobiol. Exp. (Wars) 40, 7-25.doi: 10.1007/978-94-009-8225-3_45
3. Alelú-Paz, R., and Giménez-Amaya, J. M. (2008). The mediodorsal thalamic nucleus and schizophrenia. J. Psychiatry Neurosci. 33, 489-498.
4. Alexander, G. E., and Fuster, J. M. (1973). Effects of cooling prefrontal cortex on cell firing in the nucleus medialis dorsalis. Brain Res. 61, 93-105.doi: 10.1016/0006-8993(73)90518-0
5. Alkire, M. T., Hudetz, A. G., and Tononi, G. (2008). Consciousness and anesthesia. Science 322, 876-880.doi: 10.1126/science.1149213
6. Andreasen, N. C. (1997). The role of the thalamus in schizophrenia. Can. J. Psychiatry 42, 27-33.
7. Buschman, T. J., Denovellis, E. L., Diogo, C., Bullock, D., and Miller, E. K. (2012). Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76, 838-846.doi: 10.1016/j.neuron.2012.09.029
8. 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
9. Castro-Alamancos, M. A., and Connors, B. W. (1996a). Short-term plasticity of a thalamocortical pathway dynamically modulated by behavioral state. Science 272, 274-277.doi: 10.1126/science.272.5259.274
10. Castro-Alamancos, M. A., and Connors, B. W. (1996b). Spatiotemporal properties of short-term plasticity sensorimotor thalamocortical pathways of the rat. J. Neurosci. 16, 2767-2779.
11. Chiba, T., Kayahara, T., and Nakano, K. (2001). Efferent projections of infralimbic and prelimbic areas of the medial prefrontal cortex in the Japanese monkey, Macaca fuscata. Brain Res. 888, 83-101.doi: 10.1016/s0006-8993(00)03013-4
12. 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
13. Cruikshank, S. J., Ahmed, O. J., Stevens, T. R., Patrick, S. L., Gonzalez, A. N., Elmaleh, M., et al. (2012). Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813-17823.doi: 10.1523/jneurosci.3231-12.2012
14. Di Prisco, G. V., and Vertes, R. P. (2006). Excitatory actions of the ventral midline thalamus (rhomboid/reuniens) on the medial prefrontal cortex in the rat. Synapse 60, 45-55.doi: 10.1002/syn.20271
15. Diamond, A. (2013). Executive functions. Annu. Rev. Psychol. 64, 135-168.doi: 10. 1146/annurev-psych-113011-143750
16. Dolleman-Van Der Weel, M. J., Lopes Da Silva, F. H., and Witter, M. P. (1997). Nucleus reuniens thalami modulates activity in hippocampal field CA1 through excitatory and inhibitory mechanisms. J. Neurosci. 17, 5640-5650.
17. Dolleman-Van Der, Weel, M. J., Morris, R. G., and Witter, M. P. (2009). Neu-rotoxic 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
18. Fries, P., Reynolds, J. H., Rorie, A. E., and Desimone, R. (2001). Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560-1563.doi: 10.1126/science.1055465
19. Fuster, J. M., and Alexander, G. E. (1971). Neuron activity related to short-term memory. Science 173, 652-654.doi: 10.1126/science.173.3997.652
20. Fuster, J. M., and Alexander, G. E. (1973). Firing changes in cells of the nucleus medialis dorsalis associated with delayed response behavior. Brain Res. 61, 79-91.doi: 10.1016/0006-8993(73)90517-9
21. González-Hernández, J. A., Pita-Alcorta, C., Cedeño, I., Bosch-Bayard, J., Galán-Garcia, L., Scherbaum, W. A., et al. (2002). Wisconsin Card Sorting Test synchronizes the prefrontal, temporal and posterior association cortex in different frequency ranges and extensions. Hum. Brain Mapp. 17, 37-47.doi: 10. 1002/hbm.10051
22. Gregoriou, G. G., Gotts, S. J., Zhou, H., and Desimone, R. (2009). High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324, 1207-1210.doi: 10.1126/science.1171402
23. Guillery, R. W. (1995). Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J. Anat. 187, 583-592.
24. Hembrook, J. R., Onos, K. D., and Mair, R. G. (2012). Inactivation of ventral midline thalamus produces selective spatial delayed conditional discrimination impairment in the rat. Hippocampus 22, 853-860.doi: 10.1002/hipo. 20945
25. Hoover, W. B., and Vertes, R. P. (2012). Collateral projections from nucleus reuniens of thalamus to hippocampus and medial prefrontal cortex in the rat: a single and double retrograde fluorescent labeling study. Brain Struct. Funct. 217, 191-209.doi: 10.1007/s00429-011-0345-6
26. Hudetz, A. G. (2012). General anesthesia and human brain connectivity. Brain Connect. 2, 291-302.doi: 10.1089/brain.2012.0107
27. Ichinohe, N., Mori, F., and Shoumura, K. (2000). A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat. Brain Res. 880, 191-197.doi: 10. 1016/s0006-8993(00)02744-x
28. Jones, E. G. (2007). The Thalamus. New York, NY: Cambridge University Press.
29. Kinomura, S., Larsson, J., Gulyés, B., and Roland, P. E. (1996). Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 271, 512-515.doi: 10.1126/science.271.5248.512
30. Kung, J. C., and Shyu, B. C. (2002). Potentiation of local field potentials in the anterior cingulate cortex evoked by the stimulation of the medial thalamic nuclei in rats. Brain Res. 953, 37-44.doi: 10.1016/s0006-8993(02)03265-1
31. Künzle, H., and Akert, K. (1977). Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J. Comp. Neurol. 173, 147-164.doi: 10.1002/cne.901730108
32. Liebermann, D., Ploner, C. J., Kraft, A., Kopp, U. A., and Ostendorf, F. (2013). A dysexecutive syndrome of the medial thalamus. Cortex 49, 40-49.doi: 10.1016/j. cortex.2011.11.005
33. Loureiro, M., Cholvin, T., Lopez, J., Merienne, N., Latreche, A., Cosquer, B., et al. (2012). The ventral midline thalamus (reuniens and rhomboid nuclei) contributes to the persistence of spatial memory in rats. J. Neurosci. 32, 9947-9959.doi: 10.1523/jneurosci.0410-12.2012
34. Macchi, G., Bentivoglio, M., Molinari, M., and Minciacchi, D. (1984). The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp. Brain Res. 54, 225-239.doi: 10. 1007/bf00236222
35. 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.
36. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167-202.doi: 10.1146/annurev.neuro.24. 1.167
37. Minamimoto, T., Hori, Y., and Kimura, M. (2005). Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308, 1798-1801.doi: 10.1126/science.1109154
38. Minamimoto, T., Hori, Y., Yamanaka, K., and Kimura, M. (2014). Neural signal for counteracting pre-action bias in the centromedian thalamic nucleus. Front. Syst. Neurosci. 8:3.doi: 10.3389/fnsys.2014.00003
39. Minamimoto, T., and Kimura, M. (2002). Participation of the thalamic CM-Pf complex in attentional orienting. J. Neurophysiol. 87, 3090-3101.
40. Mitchell, A. S., Browning, P. G., Wilson, C. R., Baxter, M. G., and Gaffan, D. (2008). Dissociable roles for cortical and subcortical structures in memory retrieval and acquisition. J. Neurosci. 28, 8387-8396.doi: 10.1523/jneurosci.1924-08. 2008
41. Morales, G. J., Ramcharan, E. J., Sundararaman, N., Morgera, S. D., and Vertes, R. P. (2007). Analysis of the actions of nucleus reuniens and the entorhinal cortex on EEG and evoked population behavior of the hippocampus. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 2480-2484.doi: 10.1109/iembs.2007.4352831
42. Morison, R. S., and Dempsey, E. W. (1943). Mechanism of thalamocortical augmentation and repetition. Am. J. Physiol. 138, 297-308.
43. Pandya, D. N., Van Hoesen, G. W., and Mesulam, M. M. (1981). Efferent connections of the cingulate gyrus in the rhesus monkey. Exp. Brain Res. 42, 319-330.doi: 10.1007/bf00237497
44. Paré, D., and Smith, Y. (1996). Thalamic collaterals of corticostriatal axons: their termination field and synaptic targets in cats. J. Comp. Neurol. 372, 551-567.doi: 10.1002/(sici)1096-9861(19960902)372:4551::aid-cne53.0.co;2-3
45. Parent, M., Levesque, M., and Parent, A. (2001). Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J. Comp. Neurol. 439, 162-175.doi: 10.1002/cne.1340
46. Parnaudeau, S., O'neill, P. K., Bolkan, S. S., Ward, R. D., Abbas, A. I., Roth, B. L., et al. (2013). Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition. Neuron 77, 1151-1162.doi: 10.1016/j.neuron.2013. 01.038
47. Popken, G. J., Bunney, W. E. Jr., Potkin, S. G., and Jones, E. G. (2000). Subnucleus-specific loss of neurons in medial thalamus of schizophrenics. Proc. Natl. Acad. Sci. U S A 97, 9276-9280.doi: 10.1073/pnas.150243397
48. Purushothaman, G., Marion, R., Li, K., and Casagrande, V. A. (2012). Gating and control of primary visual cortex by pulvinar. Nat. Neurosci. 15, 905-912.doi: 10. 1038/nn.3106
49. Ray, J. P., and Price, J. L. (1993). The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 337, 1-31.doi: 10.1002/cne.903370102
50. Royce, G. J. (1983a). Cortical neurons with collateral projections to both the caudate nucleus and the centromedian-parafascicular thalamic complex: a fluorescent retrograde double labeling study in the cat. Exp. Brain Res. 50, 157-165.
51. Royce, G. J. (1983b). Single thalamic neurons which project to both the rostral cortex and caudate nucleus studiedwith the fluorescent double labeling method. Exp. Neurol. 79, 773-784.doi: 10.1016/0014-4886(83)90041-9
52. Royce, G. J., Bromley, S., Gracco, C., and Beckstead, R. M. (1989). Thalamocortical connections of the rostral intralaminar nuclei: an autoradiographic analysis in the cat. J. Comp. Neurol. 288, 555-582.doi: 10.1002/cne.902880404
53. Royce, G. J., and Mourey, R. J. (1985). Efferent connections of the centromedian and parafascicular thalamic nuclei: an autoradiographic investigation in the cat. J. Comp. Neurol. 235, 277-300.doi: 10.1002/cne.902350302
54. Saalmann, Y. B., and Kastner, S. (2011). Cognitive and perceptual functions of the visual thalamus. Neuron 71, 209-223.doi: 10.1016/j.neuron.2011.06.027
55. Saalmann, Y. B., Pigarev, I. N., and Vidyasagar, T. R. (2007). Neural mechanisms of visual attention: how top-down feedback highlights relevant locations. Science 316, 1612-1615.doi: 10.1126/science.1139140
56. 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
57. Sadikot, A. F., Parent, A., and Francois, C. (1992). Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a PHA-L study of subcortical projections. J. Comp. Neurol. 315, 137-159.doi: 10. 1002/cne.903150203
58. Schiff, N. D. (2008). Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann. N Y Acad. Sci. 1129, 105-118.doi: 10.1196/annals.1417.029
59. 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
60. Schiff, N. D., Shah, S. A., Hudson, A. E., Nauvel, T., Kalik, S. F., and Purpura, K. P. (2013). Gating of attentional effort through the central thalamus. J. Neurophysiol. 109, 1152-1163.doi: 10.1152/jn.00317.2011
61. Schlag, J. (2009). "Thalamus and oculomotor control," in Encyclopedia of Neuro-science, ed L. R. Squire 1st Edn. (Waltham, Massachusetts: Academic Press), 945-953.
62. Schlag-Rey, M., and Schlag, J. (1984). Visuomotor functions of central thalamus in monkey. I. Unit activity related to spontaneous eye movements. J. Neurophysiol. 51, 1149-1174.
63. Selemon, L. D., and Goldman-Rakic, P. S. (1985). Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 5, 776-794.
64. Sherman, S. M., and Guillery, R. W. (2002). The role of the thalamus in the flow of information to the cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 1695-1708.doi: 10.1098/rstb.2002.1161
65. Sherman, S. M., and Guillery, R. W. (2006). Exploring the Thalamus and its Role in Cortical Function. Cambridge, Mass: MIT Press.
66. Shipp, S. (2003). The functional logic of cortico-pulvinar connections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1605-1624.doi: 10.1098/rstb.2002.1213
67. Siapas, A. G., Lubenov, E. V., and Wilson, M. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141-151.doi: 10.1016/j.neuron.2005.02.028
68. Smith, Y., Raju, D. V., Pare, J. F., and Sidibe, M. (2004). The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci. 27, 520-527.doi: 10.1016/j.tins.2004.07.004
69. Smith, Y., Surmeier, D. J., Redgrave, P., and Kimura, M. (2011). Thalamic contributions to basal ganglia-related behavioral switching and reinforcement. J. Neurosci. 31, 16102-16106.doi: 10.1523/jneurosci.4634-11.2011
70. Snow, J. C., Allen, H. A., Rafal, R. D., and Humphreys, G. W. (2009). Impaired attentional selection following lesions to human pulvinar: evidence for homol-ogy between human and monkey. Proc. Natl. Acad. Sci. U S A 106, 4054-4059.doi: 10.1073/pnas.0810086106
71. Starzl, T. E., and Magoun, H. W. (1951). Organization of the diffuse thalamic projection system. J. Neurophysiol. 14, 133-146.
72. Steriade, M., Timofeev, I., Grenier, F., and Durmuller, N. (1998). Role of thalamic and cortical neurons in augmenting responses and self-sustained activity: dual intracellular recordings in vivo. J. Neurosci. 18, 6425-6443.
73. Takeda, K., and Funahashi, S. (2002). Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks. J. Neurophysiol. 87, 567-588.
74. Tanibuchi, I., and Goldman-Rakic, P. S. (2003). Dissociation of spatial-, object- and sound-coding neurons in the mediodorsal nucleus of the primate thalamus. J. Neurophysiol. 89, 1067-1077.doi: 10.1152/jn.00207.2002
75. 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
76. Tiesinga, P., and Sejnowski, T. J. (2009). Cortical enlightenment: are attentional gamma oscillations driven by ING or PING? Neuron 63, 727-732.doi: 10.1016/j.neuron.2009.09.009
77. Uhlhaas, P. J., and Singer, W. (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11, 100-113.doi: 10.1038/nrn2774
78. Van der Werf, Y. D., Witter, M. P., and Groenewegen, H. J. (2002). The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 39, 107-140.doi: 10.1016/s0165-0173(02)00181-9
79. Vertes, R. P., Hoover, W. B., Do Valle, A. C., Sherman, A., and Rodriguez, J. J. (2006). Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J. Comp. Neurol. 499, 768-796.doi: 10.1002/cne.21135
80. Vertes, R. P., Hoover, W. B., Szigeti-Buck, K., and Leranth, C. (2007). Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res. Bull. 71, 601-609.doi: 10.1016/j.brainresbull.2006.12.002
81. Watanabe, Y., and Funahashi, S. (2004). Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. I. Cue-, delay- and response-period activity. J. Neurophysiol. 92, 1738-1755.doi: 10.1152/jn.00994.2003
82. Wilke, M., Turchi, J., Smith, K., Mishkin, M., and Leopold, D. A. (2010). Pulvinar inactivation disrupts selection of movement plans. J. Neurosci. 30, 8650-8659.doi: 10.1523/jneurosci.0953-10.2010
83. Womelsdorf, T., Schoffelen, J. M., Oostenveld, R., Singer, W., Desimone, R., Engel, A. K., et al. (2007). Modulation of neuronal interactions through neuronal synchronization. Science 316, 1609-1612.doi: 10.1126/science.1139597
84. Wróbel, A., Ghazaryan, A., Bekisz, M., Bogdan, W., and Kamiński, J. (2007). Two streams of attention-dependent beta activity in the striate recipient zone of cat's lateral posterior-pulvinar complex. J. Neurosci. 27, 2230-2240.doi: 10.1523/jneurosci.4004-06.2007
85. Wyder, M. T., Massoglia, D. P., and Stanford, T. R. (2003). Quantitative assessment of the timing and tuning of visual-related, saccade-related and delay period activity in primate central thalamus. J. Neurophysiol. 90, 2029-2052.doi: 10.1152/jn.00064.2003
86. Wyder, M. T., Massoglia, D. P., and Stanford, T. R. (2004). Contextual modulation of central thalamic delay-period activity: representation of visual and saccadic goals. J. Neurophysiol. 91, 2628-2648.doi: 10.1152/jn.01221.2003
87. Xu, W., and Sudhof, T. C. (2013). A neural circuit for memory specificity and generalization. Science 339, 1290-1295.doi: 10.1126/science.1229534
88. Zhang, Y., Yoshida, T., Katz, D. B., and Lisman, J. E. (2012). NMDAR antagonist action in thalamus imposes delta oscillations on the hippocampus. J. Neuro-physiol. 107, 3181-3189.doi: 10.1152/jn.00072.2012