Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain

Nature Reviews Neuroscience

Volumn 17, Issue 8, 2016, Pages 485-496

  Bliss, Tim V P ^a,b   Collingridge, Graham L ^a,c,d,e   Kaang, Bong Kiun ^a,f   Zhuo, Min ^a,d,g  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d UNIVERSITY OF TORONTO   (Canada)

^e MOUNT SINAI HOSPITAL   (Canada)

^f Seoul National University   (South Korea)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMIC ACID; KAINIC ACID RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANATOMY; ANTERIOR CINGULATE; ANXIETY; CHRONIC PAIN; FEAR; HUMAN; INTRACELLULAR SIGNALING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL; NERVE CELL PLASTICITY; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; ANIMAL; CINGULATE GYRUS; METABOLISM; PATHOPHYSIOLOGY; SYNAPSE;

ANIMALS; CHRONIC PAIN; GYRUS CINGULI; HUMANS; LONG-TERM POTENTIATION; NEURONAL PLASTICITY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 84974855915     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn.2016.68     Document Type: Review

References (147)

1. Fields H. L., & Besson J. M. R. Pain Modulation (Elsevier, 1988
2. Wall P. D. Pain: The Science of Suffering (Columbia Univ. Press, 2000
3. Zhuo M. Cortical excitation and chronic pain. Trends Neurosci. 31, 199-207 (2008
4. Sandkuhler J. Understanding LTP in pain pathways. Mol. Pain 3, 9 (2007
5. Zhuo M. Long-term potentiation in the anterior cingulate cortex and chronic pain. Phil. Trans. R. Soc. B 369, 20130146 (2014
6. Bushnell M. C., Ceko M., & Low L. A. Cognitive and emotional control of pain and its disruption in chronic pain. Nat. Rev. Neurosci. 14, 502-511 (2013
7. Apkarian A. V., Bushnell M. C., Treede R. D., & Zubieta J. K. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 9, 463-484 (2005
8. Talbot J. D., et al. Multiple representations of pain in human cerebral cortex. Science 251, 1355-1358 (1991
9. Craig A. D., Reiman E. M., Evans A., & Bushnell M. C. Functional imaging of an illusion of pain. Nature 384, 258-260 (1996
10. Eisenberger N. I., Lieberman M. D., & Williams K. D. Does rejection hurt?. An fMRI study of social exclusion. Science 302, 290-292 (2003
11. Yoshino A., et al. Sadness enhances the experience of pain via neural activation in the anterior cingulate cortex and amygdala: an fMRI study. Neuroimage 50, 1194-1201 (2010
12. Vogt B. A. Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 6, 533-544 (2005
13. Devinsky O., Morrell M. J., & Vogt B. A. Contributions of anterior cingulate cortex to behaviour. Brain 118, 279-306 (1995
14. Chen T., et al. Postsynaptic potentiation of corticospinal projecting neurons in the anterior cingulate cortex after nerve injury. Mol. Pain 10, 33 (2014
15. Wu L. J., Li X., Chen T., Ren M., & Zhuo M. Characterization of intracortical synaptic connections in the mouse anterior cingulate cortex using dual patch clamp recording. Mol. Brain 2, 32 (2009
16. Shyu B. C., & Vogt B. A. Short-term synaptic plasticity in the nociceptive thalamic-anterior cingulate pathway. Mol. Pain 5, 51 (2009
17. Dum R. P., Levinthal D. J., & Strick P. L. The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J. Neurosci. 29, 14223-14235 (2009
18. Kung J. C., & Shyu B. C. 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 (2002
19. Yang J. W., Shih H. C., & Shyu B. C. Intracortical circuits in rat anterior cingulate cortex are activated by nociceptive inputs mediated by medial thalamus. J. Neurophysiol. 96, 3409-3422 (2006
20. Delevich K., Tucciarone J., Huang Z. J., & Li B. The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J. Neurosci. 35, 5743-5753 (2015
21. Ma W., & Peschanski M. Spinal and trigeminal projections to the parabrachial nucleus in the rat: electron-microscopic evidence of a spino-ponto-amygdalian somatosensory pathway. Somatosens. Res. 5, 247-257 (1988
22. Han S., Soleiman M. T., Soden M. E., Zweifel L. S., & Palmiter R. D. Elucidating an affective pain circuit that creates a threat memory. Cell 162, 363-374 (2015
23. Eto K., et al. Inter-regional contribution of enhanced activity of the primary somatosensory cortex to the anterior cingulate cortex accelerates chronic pain behavior. J. Neurosci. 31, 7631-7636 (2011
24. Bragin E. O., et al. Cortical projections to the periaqueductal grey in the cat: a retrograde horseradish peroxidase study. Neurosci. Lett. 51, 271-275 (1984
25. LeDoux J. E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184 (2000
26. Tovote P., Fadok J. P., & Luthi A. Neuronal circuits for fear and anxiety. Nat. Rev. Neurosci. 16, 317-331 (2015
27. Medalla M., & Barbas H. The anterior cingulate cortex may enhance inhibition of lateral prefrontal cortex via m2 cholinergic receptors at dual synaptic sites. J. Neurosci. 32, 15611-15625 (2012
28. Aston-Jones G., & Cohen J. D. Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance. J. Comp. Neurol. 493, 99-110 (2005
29. Hickey L., et al. Optoactivation of locus ceruleus neurons evokes bidirectional changes in thermal nociception in rats. J. Neurosci. 34, 4148-4160 (2014
30. Chandler D. J., Lamperski C. S., & Waterhouse B. D. Identification and distribution of projections from monoaminergic and cholinergic nuclei to functionally differentiated subregions of prefrontal cortex. Brain Res. 1522, 38-58 (2013
31. Wu L. J., Zhao M. G., Toyoda H., Ko S. W., & Zhuo M. Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J. Neurophysiol. 94, 1805-1813 (2005
32. Liauw J., Wang G. D., & Zhuo M. NMDA receptors contribute to synaptic transmission in anterior cingulate cortex of adult mice. Sheng Li Xue Bao 55, 373-380 (2003
33. Wu L. J., et al. Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J. Neurosci. 25, 11107-11116 (2005
34. Kang S. J., et al. N type voltage gated calcium channels mediate excitatory synaptic transmission in the anterior cingulate cortex of adult mice. Mol. Pain 9, 58 (2013
35. Wu L. J., Xu H., Ren M., & Zhuo M. Genetic and pharmacological studies of GluR5 modulation of inhibitory synaptic transmission in the anterior cingulate cortex of adult mice. Dev. Neurobiol. 67, 146-157 (2007
36. Gronbladh A., Johansson J., Nyberg F., & Hallberg M. Recombinant human growth hormone affects the density and functionality of GABAB receptors in the male rat brain. Neuroendocrinology 97, 203-211 (2013
37. Scheperjans F., Grefkes C., Palomero-Gallagher N., Schleicher A., & Zilles K. Subdivisions of human parietal area 5 revealed by quantitative receptor autoradiography: a parietal region between motor, somatosensory, and cingulate cortical areas. Neuroimage 25, 975-992 (2005
38. Koga K., et al. In vivo whole-cell patch-clamp recording of sensory synaptic responses of cingulate pyramidal neurons to noxious mechanical stimuli in adult mice. Mol. Pain 6, 62 (2010
39. Yamamura H., et al. Morphological and electrophysiological properties of ACCx nociceptive neurons in rats. Brain Res. 735, 83-92 (1996
40. Hutchison W. D., Davis K. D., Lozano A. M., Tasker R. R., & Dostrovsky J. O. Pain-related neurons in the human cingulate cortex. Nat. Neurosci. 2, 403-405 (1999
41. Iwata K., et al. Anterior cingulate cortical neuronal activity during perception of noxious thermal stimuli in monkeys. J. Neurophysiol. 94, 1980-1991 (2005
42. Kang S. J., et al. Bidirectional modulation of hyperalgesia via the specific control of excitatory and inhibitory neuronal activity in the ACC. Mol. Brain 8, 81 (2015
43. Johansen J. P., & Fields H. L. Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat. Neurosci. 7, 398-403 (2004
44. Johansen J. P., Fields H. L., & Manning B. H. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc. Natl Acad. Sci. USA 98, 8077-8082 (2001
45. Qu C., et al. Lesion of the rostral anterior cingulate cortex eliminates the aversiveness of spontaneous neuropathic pain following partial or complete axotomy. Pain 152, 1641-1648 (2011
46. Gao Y. J., Ren W. H., Zhang Y. Q., & Zhao Z. Q. Contributions of the anterior cingulate cortex and amygdala to pain-and fear-conditioned place avoidance in rats. Pain 110, 343-353 (2004
47. LaGraize S. C., & Fuchs P. N. GABAA but not GABAB receptors in the rostral anterior cingulate cortex selectively modulate pain-induced escape/avoidance behavior. Exp. Neurol. 204, 182-194 (2007
48. Barthas F., et al. The anterior cingulate cortex is a critical hub for pain-induced depression. Biol. Psychiatry 77, 236-245 (2015
49. Donahue R. R., LaGraize S. C., & Fuchs P. N. Electrolytic lesion of the anterior cingulate cortex decreases inflammatory, but not neuropathic nociceptive behavior in rats. Brain Res. 897, 131-138 (2001
50. Gu L., et al. Pain inhibition by optogenetic activation of specific anterior cingulate cortical neurons. PLoS ONE 10, e0117746 (2015
51. Bliss T. V., & Collingridge G. L. Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide. Mol. Brain 6, 5 (2013
52. Bliss T. V., & Collingridge G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39 (1993
53. Sandkuhler J., & Gruber-Schoffnegger D. Hyperalgesia by synaptic long-term potentiation (LTP): an update. Curr. Opin. Pharmacol. 12, 18-27 (2012
54. Li X. Y., et al. Alleviating neuropathic pain hypersensitivity by inhibiting PKMζ in the anterior cingulate cortex. Science 330, 1400-1404 (2010
55. Chen T., et al. Adenylyl cyclase subtype 1 is essential for late-phase long term potentiation and spatial propagation of synaptic responses in the anterior cingulate cortex of adult mice. Mol. Pain 10, 65 (2014
56. Liauw J., Wu L. J., & Zhuo M. Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex. J. Neurophysiol. 94, 878-882 (2005
57. Zhao M. G., et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47, 859-872 (2005
58. Volianskis A., et al. Different NMDA receptor subtypes mediate induction of long-term potentiation and two forms of short-term potentiation at CA1 synapses in rat hippocampus in vitro. J. Physiol. 591, 955-972 (2013
59. Koga K., et al. Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain. Neuron 85, 377-389 (2015
60. Bortolotto Z. A., et al. Kainate receptors are involved in synaptic plasticity. Nature 402, 297-301 (1999
61. Jane D. E., Lodge D., & Collingridge G. L. Kainate receptors: pharmacology, function and therapeutic potential. Neuropharmacology 56, 90-113 (2009
62. Shin R. M., et al. Hierarchical order of coexisting pre-and postsynaptic forms of long-term potentiation at synapses in amygdala. Proc. Natl Acad. Sci. USA 107, 19073-19078 (2010
63. Alford S., Frenguelli B. G., Schofield J. G., & Collingridge G. L. Characterization of Ca2+ signals induced in hippocampal CA1 neurones by the synaptic activation of NMDA receptors. J. Physiol. 469, 693-716 (1993
64. Bliss T., Collingridge G., & Morris R. in The Hippocampus Book (eds Andersen P., Morris R., Amaral D., Bliss T., & O'Keefe J.) 343-474 (Oxford Univ. Press, 2007
65. Wei F., et al. Calmodulin regulates synaptic plasticity in the anterior cingulate cortex and behavioral responses: a microelectroporation study in adult rodents. J. Neurosci. 23, 8402-8409 (2003
66. Xia Z., & Storm D. R. Calmodulin-regulated adenylyl cyclases and neuromodulation. Curr. Opin. Neurobiol. 7, 391-396 (1997
67. Wei F., et al. Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Neuron 36, 713-726 (2002
68. Wang H., et al. Identification of an adenylyl cyclase inhibitor for treating neuropathic and inflammatory pain. Sci. Transl. Med. 3, 65ra63 (2011
69. Wei F., et al. Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat. Neurosci. 5, 573-579 (2002
70. Jones M. W., et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4, 289-296 (2001
71. Ko S. W., et al. Transcription factor Egr 1 is required for long-term fear memory and anxiety. Sheng Li Xue Bao 57, 421-432 (2005
72. Zalfa F., et al. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112, 317-327 (2003
73. Zhao M. G., et al. Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J. Neurosci. 25, 7385-7392 (2005
74. Toyoda H., et al. Requirement of extracellular signal-regulated kinase/mitogen-activated protein kinase for long-term potentiation in adult mouse anterior cingulate cortex. Mol. Pain 3, 36 (2007
75. Nicoll R. A., & Schmitz D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6, 863-876 (2005
76. Koga K., et al. Impaired presynaptic long-term potentiation in the anterior cingulate cortex of Fmr1 knock-out mice. J. Neurosci. 35, 2033-2043 (2015
77. Hayashi Y., et al. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267 (2000
78. Passafaro M., Piech V., & Sheng M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4, 917-926 (2001
79. Toyoda H., Wu L. J., Zhao M. G., Xu H., & Zhuo M. Time-dependent postsynaptic AMPA GluR1 receptor recruitment in the cingulate synaptic potentiation. Dev. Neurobiol. 67, 498-509 (2007
80. Toyoda H., et al. Roles of the AMPA receptor subunit GluA1 but not GluA2 in synaptic potentiation and activation of ERK in the anterior cingulate cortex. Mol. Pain 5, 46 (2009
81. Plant K., et al. Transient incorporation of native GluR2 lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604 (2006
82. Park P., et al. Calcium-permeable AMPA receptors mediate the induction of the protein kinase A dependent component of long-term potentiation in the hippocampus. J. Neurosci. 36, 622-631 (2016
83. Sacktor T. C. Memory maintenance by PKMζ - an evolutionary perspective. Mol. Brain 5, 31 (2012
84. Yao Y., et al. PKMζ maintains late long-term potentiation by N ethylmaleimide-sensitive factor/GluR2 dependent trafficking of postsynaptic AMPA receptors. J. Neurosci. 28, 7820-7827 (2008
85. Volk L. J., Bachman J. L., Johnson R., Yu Y., & Huganir R. L. PKM-ζ is not required for hippocampal synaptic plasticity, learning and memory. Nature 493, 420-423 (2013
86. Lee A. M., et al. Prkcz null mice show normal learning and memory. Nature 493, 416-419 (2013
87. Tsokas P., et al. Compensation for PKMζ in long-term potentiation and spatial long-term memory in mutant mice. eLife 5, e14846 (2016
88. Mellor J., Nicoll R. A., & Schmitz D. Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science 295, 143-147 (2002
89. Chevaleyre V., & Castillo P. E. Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc. Natl Acad. Sci. USA 99, 9538-9543 (2002
90. Collingridge G. L., Peineau S., Howland J. G., & Wang Y. T. Long-term depression in the CNS. Nat. Rev. Neurosci. 11, 459-473 (2010
91. Wei F., Li P., & Zhuo M. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J. Neurosci. 19, 9346-9354 (1999
92. Kang S. J., et al. Plasticity of metabotropic glutamate receptor-dependent long-term depression in the anterior cingulate cortex after amputation. J. Neurosci. 32, 11318-11329 (2012
93. Toyoda H., Zhao M. G., & Zhuo M. Roles of NMDA receptor NR2A and NR2B subtypes for long-term depression in the anterior cingulate cortex. Eur. J. Neurosci. 22, 485-494 (2005
94. Toyoda H., et al. Long-term depression requires postsynaptic AMPA GluR2 receptor in adult mouse cingulate cortex. J. Cell. Physiol. 211, 336-343 (2007
95. Wei F., & Zhuo M. Activation of Erk in the anterior cingulate cortex during the induction and expression of chronic pain. Mol. Pain 4, 28 (2008
96. Wu M. F., Pang Z. P., Zhuo M., & Xu Z. C. Prolonged membrane potential depolarization in cingulate pyramidal cells after digit amputation in adult rats. Mol. Pain 1, 23 (2005
97. Wei F., & Zhuo M. Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat. J. Physiol. 532, 823-833 (2001
98. Chiou C. S., Huang C. C., Liang Y. C., Tsai Y. C., & Hsu K. S. Impairment of long-term depression in the anterior cingulate cortex of mice with bone cancer pain. Pain 153, 2097-2108 (2012
99. Xu H., et al. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J. Neurosci. 28, 7445-7453 (2008
100. Zhao M. G., et al. Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J. Neurosci. 26, 8923-8930 (2006
101. Bie B., Brown D. L., & Naguib M. Increased synaptic GluR1 subunits in the anterior cingulate cortex of rats with peripheral inflammation. Eur. J. Pharmacol. 653, 26-31 (2011
102. Chen T., et al. Postsynaptic insertion of AMPA receptor onto cortical pyramidal neurons in the anterior cingulate cortex after peripheral nerve injury. Mol. Brain 7, 76 (2014
103. Hartmann B., et al. The AMPA receptor subunits GluR A and GluR B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 44, 637-650 (2004
104. Yang J. X., et al. Caveolin 1 in the anterior cingulate cortex modulates chronic neuropathic pain via regulation of NMDA receptor 2B subunit. J. Neurosci. 35, 36-52 (2015
105. Metz A. E., Yau H. J., Centeno M. V., Apkarian A. V., & Martina M. Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. Proc. Natl Acad. Sci. USA 106, 2423-2428 (2009
106. Qiu S., et al. An increase in synaptic NMDA receptors in the insular cortex contributes to neuropathic pain. Sci. Signal. 6, ra34 (2013
107. Niikura K., et al. Enhancement of glutamatergic transmission in the cingulate cortex in response to mild noxious stimuli under a neuropathic pain-like state. Synapse 65, 424-432 (2011
108. Cao X. Y., et al. Characterization of intrinsic properties of cingulate pyramidal neurons in adult mice after nerve injury. Mol. Pain 5, 73 (2009
109. Li X. Y., et al. Long-term temporal imprecision of information coding in the anterior cingulate cortex of mice with peripheral inflammation or nerve injury. J. Neurosci. 34, 10675-10687 (2014
110. Zhang M. M., et al. Effects of NB001 and gabapentin on irritable bowel syndrome-induced behavioral anxiety and spontaneous pain. Mol. Brain 7, 47 (2014
111. Zhuo M. Targeting neuronal adenylyl cyclase for the treatment of chronic pain. Drug Discov. Today 17, 573-582 (2012
112. Descalzi G., Fukushima H., Suzuki A., Kida S., & Zhuo M. Genetic enhancement of neuropathic and inflammatory pain by forebrain upregulation of CREB-mediated transcription. Mol. Pain 8, 90 (2012
113. Wu L. J., et al. Enhancement of presynaptic glutamate release and persistent inflammatory pain by increasing neuronal cAMP in the anterior cingulate cortex. Mol. Pain 4, 40 (2008
114. Rumpel S., LeDoux J., Zador A., & Malinow R. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308, 83-88 (2005
115. Tang J., et al. Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol. Pain 1, 6 (2005
116. Steenland H. W., Li X. Y., & Zhuo M. Predicting aversive events and terminating fear in the mouse anterior cingulate cortex during trace fear conditioning. J. Neurosci. 32, 1082-1095 (2012
117. Bonin R. P., & De Koninck Y. A spinal analog of memory reconsolidation enables reversal of hyperalgesia. Nat. Neurosci. 17, 1043-1045 (2014
118. Bonin R. P., & De Koninck Y. Reconsolidation and the regulation of plasticity: moving beyond memory. Trends Neurosci. 38, 336-344 (2015
119. Bissiere S., et al. The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning. Biol. Psychiatry 63, 821-831 (2008
120. Jeon D., et al. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat. Neurosci. 13, 482-488 (2010
121. Descalzi G., et al. Rapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning. Mol. Brain 5, 6 (2012
122. Knight D. C., Cheng D. T., Smith C. N., Stein E. A., & Helmstetter F. J. Neural substrates mediating human delay and trace fear conditioning. J. Neurosci. 24, 218-228 (2004
123. Frankland P. W., Bontempi B., Talton L. E., Kaczmarek L., & Silva A. J. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304, 881-883 (2004
124. Ploghaus A., et al. Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J. Neurosci. 21, 9896-9903 (2001
125. Kain Z. N., Mayes L. C., Caldwell-Andrews A. A., Karas D. E., & McClain B. C. Preoperative anxiety, postoperative pain, and behavioral recovery in young children undergoing surgery. Pediatrics 118, 651-658 (2006
126. Myers B., & Greenwood-Van Meerveld B. Role of anxiety in the pathophysiology of irritable bowel syndrome: importance of the amygdala. Front. Neurosci. 3, 47 (2009
127. Wise R. G., et al. The anxiolytic effects of midazolam during anticipation to pain revealed using fMRI. Magn. Reson. Imag. 25, 801-810 (2007
128. Osuch E. A., et al. Regional cerebral metabolism associated with anxiety symptoms in affective disorder patients. Biol. Psychiatry 48, 1020-1023 (2000
129. Hubbard C. S., et al. Behavioral, metabolic and functional brain changes in a rat model of chronic neuropathic pain: a longitudinal MRI study. Neuroimage 107, 333-344 (2015
130. Robbins M., DeBerry J., & Ness T. Chronic psychological stress enhances nociceptive processing in the urinary bladder in high-anxiety rats. Physiol. Behav. 91, 544-550 (2007
131. Gabbott P. L., Warner T. A., Jays P. R., Salway P., & Busby S. J. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 492, 145-177 (2005
132. Cassell M. D., & Wright D. J. Topography of projections from the medial prefrontal cortex to the amygdala in the rat. Brain Res. Bull. 17, 321-333 (1986
133. Buchanan S. L., Thompson R. H., Maxwell B. L., & Powell D. A. Efferent connections of the medial prefrontal cortex in the rabbit. Exp. Brain Res. 100, 469-483 (1994
134. Kim S. S., et al. Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice. Mol. Brain 4, 6 (2011
135. Ruscheweyh R., Wilder-Smith O., Drdla R., Liu X. G., & Sandkuhler J. Long-term potentiation in spinal nociceptive pathways as a novel target for pain therapy. Mol. Pain 7, 20 (2011
136. Sandkuhler J., & Liu X. Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur. J. Neurosci. 10, 2476-2480 (1998
137. Ikeda H., et al. Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312, 1659-1662 (2006
138. Guilbaud G., Benoist J. M., Jazat F., & Gautron M. Neuronal responsiveness in the ventrobasal thalamic complex of rats with an experimental peripheral mononeuropathy. J. Neurophysiol. 64, 1537-1554 (1990
139. Zhao P., Waxman S. G., & Hains B. C. Sodium channel expression in the ventral posterolateral nucleus of the thalamus after peripheral nerve injury. Mol. Pain 2, 27 (2006
140. Guilbaud G., Kayser V., Benoist J. M., & Gautron M. Modifications in the responsiveness of rat ventrobasal thalamic neurons at different stages of carrageenin-produced inflammation. Brain Res. 385, 86-98 (1986
141. Neugebauer V., Li W., Bird G. C., Bhave G., & Gereau R. W. Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5. J. Neurosci. 23, 52-63 (2003
142. Ikeda R., Takahashi Y., Inoue K., & Kato F. NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. Pain 127, 161-172 (2007
143. Nakao A., Takahashi Y., Nagase M., Ikeda R., & Kato F. Role of capsaicin-sensitive C fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala. Mol. Pain 8, 51 (2012
144. Liu M. G., et al. Long-term depression of synaptic transmission in the adult mouse insular cortex in vitro. Eur. J. Neurosci. 38, 3128-3145 (2013
145. Liu M. G., et al. Long-term potentiation of synaptic transmission in the adult mouse insular cortex: multielectrode array recordings. J. Neurophysiol. 110, 505-521 (2013
146. Qiu S., et al. GluA1 phosphorylation contributes to postsynaptic amplification of neuropathic pain in the insular cortex. J. Neurosci. 34, 13505-13515 (2014
147. Liu M. G., & Zhuo M. No requirement of TRPV1 in long-term potentiation or long-term depression in the anterior cingulate cortex. Mol. Brain 7, 27 (2014