Pathways for emotions and attention converge on the thalamic reticular nucleus in primates

Journal of Neuroscience

Volumn 32, Issue 15, 2012, Pages 5338-5350

  Zikopoulos, Basilis ^a   Barbas, Helen ^a,b  

^a BOSTON UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRACER;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMOTION; FEMALE; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MALE; MICROSCOPY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ORBITAL CORTEX; PRIORITY JOURNAL; THALAMUS DORSOMEDIAL NUCLEUS; THALAMUS RETICULAR NUCLEUS;

AMYGDALA; ANIMALS; ATTENTION; EMOTIONS; FEMALE; FRONTAL LOBE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MEDIODORSAL THALAMIC NUCLEUS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; THALAMIC NUCLEI;

EID: 84859550771     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/jneurosci.4793-11.2012     Document Type: Article

References (97)

1. Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56-68
2. Amaral DG, Behniea H, Kelly JL (2003) Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 118:1099-1120
3. Anderson AK, Christoff K, Panitz D, De Rosa E, Gabrieli JD (2003) Neural correlates of the automatic processing of threat facial signals. J Neurosci 23:5627-5633
4. Arnsten AF (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410-422
5. Barbas H (2007) Flow of information for emotions through temporal and orbitofrontal pathways. J Anat 211:237-249
6. Barbas H, Zikopoulos B (2006) Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex. In: The orbitofrontal cortex (David Zald, Scott Rauch, eds), pp 57-91 Oxford: Oxford UP.
7. Barbas H, Zikopoulos B (2007) The prefrontal cortex and flexible behavior. Neuroscientist 13:532-545
8. Barbas H, Henion TH, Dermon CR (1991) Diverse thalamic projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 313:65-94
9. Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69:1133-1139
10. Bechara A, Damasio H, Damasio AR (2000) Emotion, decision making and the orbitofrontal cortex. Cereb Cortex 10:295-307
11. Benes FM (2010) Amygdalocortical circuitry in schizophrenia: from circuits to molecules. Neuropsychopharmacology 35:239-257
12. Berezhnaya LA (2006) Neuronal organization of the reticular nucleus of the thalamus in adult humans. Neurosci Behav Physiol 36:519-525
13. Bishop SJ (2008) Neural mechanisms underlying selective attention to threat. Ann N Y Acad Sci 1129:141-152
14. Browning M, Holmes EA, Harmer CJ (2010) The modification of attentional bias to emotional information: A review of the techniques, mechanisms, and relevance to emotional disorders. Cogn Affect Behav Neurosci 10:8-20
15. Bunce JG, Barbas H (2011) Prefrontal pathways target excitatory and inhibitory systems in memory-related medial temporal cortices. Neuroimage 55:1461-1474
16. Cavada C, Compañy T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suárez F (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 10:220-242
17. Compton RJ (2003) The interface between emotion and attention: a review of evidence from psychology and neuroscience. Behav Cogn Neurosci Rev 2:115-129
18. Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci U S A 81:4586-4590
19. Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51:68-80
20. De Olmos JS (1990) Amygdala. In: The human nervous system (Paxinos G, ed), pp 583-710 San Diego: Academic.
21. Del Casale A, Kotzalidis GD, Rapinesi C, Serata D, Ambrosi E, Simonetti A, Pompili M, Ferracuti S, Tatarelli R, Girardi P (2011) Functional neuroimaging in obsessive-compulsive disorder. Neuropsychobiology 64:61-85.
22. Dermon CR, Barbas H (1994) Contralateral thalamic projections predominantly reach transitional cortices in the rhesus monkey. J Comp Neurol 344:508-531
23. Feldman ML, Peters A (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J Comp Neurol 179:761-793
24. Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218:52-61
25. Franks KM, Stevens CF, Sejnowski TJ (2003) Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23:3186-3195
26. Fuentealba P, Steriade M (2005) The reticular nucleus revisited: Intrinsic and network properties of a thalamic pacemaker. Prog Neurobiol 75:125-141
27. Germuska M, Saha S, Fiala J, Barbas H (2006) Synaptic distinction of laminar specific prefrontal-temporal pathways in primates. Cereb Cortex 16:865-875
28. Ghashghaei HT, Barbas H (2002) Pathways for emotions: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261-1279
29. Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34:905-923
30. Giguere M, Goldman-Rakic PS (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
31. Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242:535-560
32. Greenberg BD, Rauch SL, Haber SN (2010) Invasive circuitry-based neurotherapeutics: stereotactic ablation and deep brain stimulation for OCD. Neuropsychopharmacology 35:317-336
33. Guillery RW, Harting JK (2003) Structure and connections of the thalamic reticular nucleus: advancing views over half a century. J Comp Neurol 463:360-371
34. Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2:e22.
35. Höistad M, Barbas H (2008) Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala. Neuroimage 40:1016-1033
36. Holtzheimer PE, Mayberg HS (2011) Deep brain stimulation for psychiatric disorders. Annu Rev Neurosci 34:289-307
37. Jones EG (2007) The thalamus. New York: Cambridge UP.
38. Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, Marchante AN, Whalen PJ (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223:403-410
39. Koechlin E, Hyafil A (2007) Anterior prefrontal function and the limits of human decision-making. Science 318:594-598
40. Lam YW, Sherman SM (2005) Mapping by laser photostimulation of connections between the thalamic reticular and ventral posterior lateral nuclei in the rat. J Neurophysiol 94:2472-2483
41. Lanuza E, Nader K, Ledoux JE (2004) Unconditioned stimulus pathways to the amygdala: effects of posterior thalamic and cortical lesions on fear conditioning. Neuroscience 125:305-315
42. Lanuza E, Moncho-Bogani J, Ledoux JE (2008) Unconditioned stimulus pathways to the amygdala: Effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala. Neuroscience 155:959-968
43. Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43
44. Liu XB, Jones EG (1999) Predominance of corticothalamic synaptic inputs to thalamic reticular nucleus neurons in the rat. J Comp Neurol 414:67-79
45. Mathews A, Mackintosh B, Fulcher EP (1997) Cognitive biases in anxiety and attention to threat. Trends Cogn Sci 1:340-345
46. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, Schwalb JM, Kennedy SH (2005) Deep brain stimulation for treatmentresistant depression. Neuron 45:651-660
47. McAlonan K, Cavanaugh J, Wurtz RH (2008) Guarding the gateway to cortex with attention in visual thalamus. Nature 456:391-394
48. McDonald AJ (1987) Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: a fluorescence retrograde transport study in the rat. J Comp Neurol 262:46-58
49. McKenna JT, Vertes RP (2004) Afferent projections to nucleus reuniens of the thalamus. J Comp Neurol 480:115-142
50. Medalla M, Barbas H (2009) Synapses with inhibitory neurons differentiate anterior cingulate from dorsolateral prefrontal pathways associated with cognitive control. Neuron 61:609-620
51. Medalla M, Barbas H (2010) Anterior cingulate synapses in prefrontal areas 10 and 46 suggest differential influence in cognitive control. J Neurosci 30:16068-16081.
52. Mitchell DG, Luo Q, Mondillo K, Vythilingam M, Finger EC, Blair RJ (2008) The interference of operant task performance by emotional distracters: an antagonistic relationship between the amygdala and frontoparietal cortices. Neuroimage 40:859-868
53. Miyashita T, Ichinohe N, Rockland KS (2007) Differential modes of termination of amygdalothalamic and amygdalocortical projections in the monkey. J Comp Neurol 502:309-324
54. Montero VM (1997) c-fos induction in sensory pathways of rats exploring a novel complex environment: shifts of active thalamic reticular sectors by predominant sensory cues. Neuroscience 76:1069-1081
55. Morris JS, Friston KJ, Buchel C, Frith CD, Young AW, Calder AJ, Dolan RJ (1998) A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121:47-57
56. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599-612
57. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673-682
58. Nakatani T (1993) The degree of GABA immunoreactivity is related to neuronal size in the thalamic reticular nucleus of the Japanese monkey, Macaca fuscata. Kaibogaku Zasshi 68:180-189
59. Nonkes LJ, Tomson K, Maertin A, Dederen J, Maes JH, Homberg J (2010) Orbitofrontal cortex and amygdalar over-activity is associated with an inability to use the value of expected outcomes to guide behaviour in serotonin transporter knockout rats. Neurobiol Learn Mem 94:65-72
60. Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2:417-424
61. Pessoa L (2005) To what extent are emotional visual stimuli processed without attention and awareness? Curr Opin Neurobiol 15:188-196
62. Pessoa L (2008) On the relationship between emotion and cognition. Nat Rev Neurosci 9:148-158
63. Pessoa L (2009) How do emotion and motivation direct executive control? Trends Cogn Sci 13:160-166
64. Pessoa L (2010) Emotion and cognition and the amygdala: from "what is it?" to "what's to be done?" Neuropsychologia 48:3416-3429
65. Pessoa L, Adolphs R (2010) Emotion processing and the amygdala: from a "low road" to "many roads" of evaluating biological significance. Nat Rev Neurosci 11:773-783
66. Pessoa L, Ungerleider LG (2004) Neuroimaging studies of attention and the processing of emotion-laden stimuli. Prog Brain Res 144:171-182
67. Petrof I, Brown VJ (2010) Attention to visual, but not tactile, properties of a stimulus results in activation of FOS protein in the visual thalamic reticular nucleus of rats. Behav Brain Res 211:248-252
68. Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374:387-420
69. Pierce JP, Lewin GR (1994) An ultrastructural size principle. Neuroscience 58:441-446
70. Pinault D (2004) The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev 46:1-31
71. Pinault D, Deschênes M (1998) Anatomical evidence for a mechanism of lateral inhibition in the rat thalamus. Eur J Neurosci 10:3462-3469
72. Porrino LJ, Crane AM, Goldman-Rakic PS (1981) Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. J Comp Neurol 198:121-136
73. Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242-1259
74. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG (2000) Pathway tracing using biotinylated dextran amines. J Neurosci Methods 103:23-37
75. Ressler KJ, Mayberg HS (2007) Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci 10:1116-1124
76. Rockland KS, Andresen J, Cowie RJ, Robinson DL (1999) Single axon analysis of pulvinocortical connections to several visual areas in the macaque. J Comp Neurol 406:221-250
77. Romanski LM, LeDoux JE (1992) Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J Neurosci 12:4501-4509
78. Rouiller EM, Durif C (2004) The dual pattern of corticothalamic projection of the primary auditory cortex in macaque monkey. Neurosci Lett 358:49-52
79. Rouiller EM, Welker E (1991) Morphology of corticothalamic terminals arising from the auditory cortex of the rat: a Phaseolus vulgarisleucoagglutinin (PHA-L) tracing study. Hear Res 56:179-190
80. Rouiller EM, Welker E (2000) A comparative analysis of the morphology of corticothalamic projections in mammals. Brain Res Bull 53:727-741
81. Rouiller EM, Tanné J, Moret V, Kermadi I, Boussaoud D, Welker E (1998) Dual morphology and topography of the corticothalamic terminals originating from the primary, supplementary motor, and dorsal premotor cortical areas in macaque monkeys. J Comp Neurol 396:169-185
82. Ruffini C, Locatelli M, Lucca A, Benedetti F, Insacco C, Smeraldi E (2009) Augmentation effect of repetitive transcranial magnetic stimulation over the orbitofrontal cortex in drug-resistant obsessive-compulsive disorder patients: a controlled investigation. Prim Care Companion J Clin Psychiatry 11:226-230
83. Russchen FT, Amaral DG, Price JL (1987) The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J Comp Neurol 256:175-210
84. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS (2002) Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 51:693-707
85. Stein MB, Simmons AN, Feinstein JS, Paulus MP (2007) Increased amygdala and insula activation during emotion processing in anxietyprone subjects. Am J Psychiatry 164:318-327
86. Straube T, Mentzel HJ, Miltner WH (2007) Waiting for spiders: brain activation during anticipatory anxiety in spider phobics. Neuroimage 37:1427-1436
87. Swadlow HA, Gusev AG, Bezdudnaya T (2002) Activation of a cortical column by a thalamocortical impulse. J Neurosci 22:7766-7773
88. Ulfig N, Nickel J, Bohl J (1998) Transient features of the thalamic reticular nucleus in the human foetal brain. Eur J Neurosci 10:3773-3784
89. Ursu S, Carter CS (2009) An initial investigation of the orbitofrontal cortex hyperactivity in obsessive-compulsive disorder: exaggerated representations of anticipated aversive events? Neuropsychologia 47:2145-2148
90. Vuilleumier P (2005) How brains beware: neural mechanisms of emotional attention. Trends Cogn Sci 9:585-594
91. Weese GD, Phillips JM, Brown VJ (1999) Attentional orienting is impaired by unilateral lesions of the thalamic reticular nucleus in the rat. J Neurosci 19:10135-10139.
92. Williams LM, Das P, Liddell BJ, Kemp AH, Rennie CJ, Gordon E (2006) Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. J Neurosci 26:9264-9271
93. Xiao D, Zikopoulos B, Barbas H (2009) Laminar and modular organization of prefrontal projections to multiple thalamic nuclei. Neuroscience 161:1067-1081
94. Zald DH (2003) The human amygdala and the emotional evaluation of sensory stimuli. Brain Res Brain Res Rev 41:88-123
95. Zikopoulos B, Barbas H (2006) Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J Neurosci 26:7348-7361
96. Zikopoulos B, Barbas H (2007a) Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci 18:417-438
97. Zikopoulos B, Barbas H (2007b) Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLoS One 2:e848.