Activation of corticostriatal circuitry relieves chronic neuropathic pain

Journal of Neuroscience

Volumn 35, Issue 13, 2015, Pages 5247-5259

  Lee, Michelle ^a   Manders, Toby R ^a   Eberle, Sarah E ^a   Su, Chen ^a   D’Amour, James ^a,b   Yang, Runtao ^a   Lin, Hau Yueh ^a   Deisseroth, Karl ^a,c   Froemke, Robert C ^a,b   Wang, Jing ^a,b  

^a Department of Anesthesiology ^*  (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Affective; Nucleus accumbens; Optogenetics; Pain; Prefrontal cortex

Indexed keywords

2 ,3 DIHYDROXY 6 NITRO 7 SULFAMOYL BENZO[F]QUINOXALINE 2,3 DIONE; PARVOVIRUS VECTOR; QUINOXALINE DERIVATIVE; UNCLASSIFIED DRUG;

ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BEHAVIOR ASSESSMENT; COLD ALLODYNIA TEST; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPERIMENTAL PAIN TEST; HARGREAVES TEST; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MECHANICAL ALLODYNIA TEST; NEUROPATHIC PAIN; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; PAIN ASSESSMENT; PHOTOACTIVATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STEREOTACTIC PROCEDURE; SYNAPTIC TRANSMISSION; ANIMAL; ANIMAL BEHAVIOR; CYTOLOGY; NERVE TRACT; NEURALGIA; PAIN MEASUREMENT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; MALE; NEURAL PATHWAYS; NEURALGIA; NUCLEUS ACCUMBENS; OPTOGENETICS; PAIN MEASUREMENT; PREFRONTAL CORTEX; RATS;

EID: 84929376646     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3494-14.2015     Document Type: Article

References (100)

1. Apkarian AV, Sosa Y, Sonty S, Levy RM, Harden RN, Parrish TB, Gitelman DR (2004) Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J Neurosci 24:10410–10415.
2. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9:463–484.
3. Arai A, Kessler M, Xiao P, Ambros-Ingerson J, Rogers G, Lynch G (1994) A centrally active drug that modulates AMPA receptor gated currents. Brain Res 638:343–346.
4. Arnsten AF, Wang MJ, Paspalas CD (2012) Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses. Neuron 76:223–239.
5. Bair MJ, Robinson RL, Katon W, Kroenke K (2003) Depression and pain comorbidity: a literature review. Arch Intern Med 163:2433–2445.
6. Balconi M, Ferrari C (2012) rTMS stimulation on left DLPFC increases the correct recognition of memories for emotional target and distractor words. Cogn Affect Behav Neurosci 12:589–598.
7. Baliki MN, Chialvo DR, Geha PY, Levy RM, Harden RN, Parrish TB, Apkarian AV (2006) Chronic pain and the emotional brain: specific brain activity associated with spontaneous fluctuations of intensity of chronic back pain. J Neurosci 26:12165–12173.
8. Baliki MN, Geha PY, Fields HL, Apkarian AV (2010) Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain. Neuron 66:149–160.
9. Baliki MN, Petre B, Torbey S, Herrmann KM, Huang L, Schnitzer TJ, Fields HL, Apkarian AV (2012) Corticostriatal functional connectivity predicts transition to chronic back pain. Nat Neurosci 15:1117–1119.
10. Becerra L, Borsook D (2008) Signal valence in the nucleus accumbens to pain onset and offset. Eur J Pain 12:866–869.
11. Becerra L, Breiter HC, Wise R, Gonzalez RG, Borsook D (2001) Reward circuitry activation by noxious thermal stimuli. Neuron 32:927–946.
12. Beckstead RM, Norgren R (1979) An autoradiographic examination of the central distribution of the trigeminal, facial, glossopharyngeal, and vagal nerves in the monkey. J Comp Neurol 184:455–472.
13. Bishop S, Duncan J, Brett M, Lawrence AD (2004) Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nat Neurosci 7:184–188.
14. Bissière S, Plachta N, Hoyer D, McAllister KH, Olpe HR, Grace AA, Cryan JF (2008) The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning. Biol Psychiatry 63:821–831.
15. Bourquin AF, Süveges M, Pertin M, Gilliard N, Sardy S, Davison AC, Spahn DR, Decosterd I (2006) Assessment and analysis of mechanical allodynia-like behavior induced by spared nerve injury (SNI) in the mouse. Pain 122:14.e1–14.
16. Boyce-Rustay JM, Zhong C, Kohnken R, Baker SJ, Simler GH, Wensink EJ, Decker MW, Honore P (2010) Comparison of mechanical allodynia and the affective component of inflammatory pain in rats. Neuropharmacology 58:537–543.
17. Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993) The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338:255–278.
18. Bushnell MC, Ceko M, Low LA (2013) Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 14:502–511.
19. Cardoso-Cruz H, Sousa M, Vieira JB, Lima D, Galhardo V (2013) Prefrontal cortex and mediodorsal thalamus reduced connectivity is associated with spatial working memory impairment in rats with inflammatory pain. Pain 154:2397–2406.
20. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55–63.
21. Chaudhury D, Walsh JJ, Friedman AK, Juarez B, Ku SM, Koo JW, Ferguson D, Tsai HC, Pomeranz L, Christoffel DJ, Nectow AR, Ekstrand M, Domingos A, Mazei-Robison MS, Mouzon E, Lobo MK, Neve RL, Friedman JM, Russo SJ, Deisseroth K, et al. (2013) Rapid regulation of depressionrelated behaviours by control of midbrain dopamine neurons. Nature 493:532–536.
22. Cooper SJ (1975) Anaesthetisation of prefrontal cortex and response to noxious stimulation. Nature 254:439–440.
23. Corcoran KA, Quirk GJ (2007) Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 27:840–844.
24. Damgaard T, Larsen DB, Hansen SL, Grayson B, Neill JC, Plath N (2010) Positive modulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors reverses sub-chronic PCP-induced deficits in the novel object recognition task in rats. Behav Brain Res 207:144–150.
25. Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87:149–158.
26. Deer TR, Mekhail N, Provenzano D, Pope J, Krames E, Thomson S, Raso L, Burton A, DeAndres J, Buchser E, Buvanendran A, Liem L, Kumar K, Rizvi S, Feler C, Abejon D, Anderson J, Eldabe S, Kim P, Leong M, et al. (2014) The appropriate use of neurostimulation: avoidance and treatment of complications of neurostimulation therapies for the treatment of chronic pain. Neuromodulation 17:571–598.
27. De Felice M, Eyde N, Dodick D, Dussor GO, Ossipov MH, Fields HL, Porreca F (2013) Capturing the aversive state of cephalic pain preclinically. Ann Neurol 74:257–265.
28. Dworkin RH, Gitlin MJ (1991) Clinical aspects of depression in chronic pain patients. Clin J Pain 7:79–94.
29. Edwards RR, Haythornthwaite JA, Smith MT, Klick B, Katz JN (2009) Catastrophizing and depressive symptoms as prospective predictors of outcomes following total knee replacement. Pain Res Manag 14:307–311.
30. Fenno L, Yizhar O, Deisseroth K (2011) The development and application of optogenetics. Annu Rev Neurosci 34:389–412.
31. Fields HL, Bry J, Hentall I, Zorman G (1983) The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 3:2545–2552.
32. Fishbain DA, Cutler R, Rosomoff HL, Rosomoff RS (1997) Chronic painassociated depression: antecedent or consequence of chronic pain? A review. Clin J Pain 13:116–137.
33. Fox MD, Buckner RL, White MP, Greicius MD, Pascual-Leone A (2012) Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biol Psychiatry 72:595–603.
34. Fuster JM (2009) Cortex and memory: emergence of a new paradigm. J Cogn Neurosci 21:2047–2072.
35. Gear RW, Levine JD (2009) Rostral ventral medulla cholinergic mechanism in pain-induced analgesia. Neurosci Lett 464:170–172.
36. Gear RW, Aley KO, Levine JD (1999) Pain-induced analgesia mediated by mesolimbic reward circuits. J Neurosci 19:7175–7181.
37. Geha PY, Baliki MN, Harden RN, Bauer WR, Parrish TB, Apkarian AV (2008) The brain in chronic CRPS pain: abnormal gray-white matter interactions in emotional and autonomic regions. Neuron 60:570–581.
38. Goff DC, Lamberti JS, Leon AC, Green MF, Miller AL, Patel J, Manschreck T, Freudenreich O, Johnson SA (2008) A placebo-controlled add-on trial of the Ampakine, CX516, for cognitive deficits in schizophrenia. Neuropsychopharmacology 33:465–472.
39. Goffer Y, Xu D, Eberle SE, D’amour J, Lee M, Tukey D, Froemke RC, Ziff EB, Wang J (2013) Calcium-permeable AMPA receptors in the nucleus accumbens regulate depression-like behaviors in the chronic neuropathic pain state. J Neurosci 33:19034–19044.
40. Gonçalves L, Silva R, Pinto-Ribeiro F, Pêgo JM, Bessa JM, Pertovaara A, Sousa N, Almeida A (2008) Neuropathic pain is associated with depressive behaviour and induces neuroplasticity in the amygdala of the rat. Exp Neurol 213:48–56.
41. Hao JX, Shi TJ, Xu IS, Kaupilla T, Xu XJ, Hökfelt T, Bartfai T, Wiesenfeld Hallin Z (1999) Intrathecal galanin alleviates allodynia-like behaviour in rats after partial peripheral nerve injury. Eur J Neurosci 11:427–432.
42. Hardy SG (1985) Analgesia elicited by prefrontal stimulation. Brain Res 339:281–284.
43. Hardy SG, Haigler HJ (1985) Prefrontal influences upon the midbrain: a possible route for pain modulation. Brain Res 339:285–293.
44. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77–88.
45. Holtzheimer PE, Kelley ME, Gross RE, Filkowski MM, Garlow SJ, Barrocas A, Wint D, Craighead MC, Kozarsky J, Chismar R, Moreines JL, Mewes K, Posse PR, Gutman DA, Mayberg HS (2012) Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression. Arch Gen Psychiatry 69:150–158.
46. Hu B, Doods H, Treede RD, Ceci A (2009) Depression-like behaviour in rats with mononeuropathy is reduced by the CB2-selective agonist GW405833. Pain 143:206–212.
47. Hung KL, Wang SJ, Wang YC, Chiang TR, Wang CC (2014) Upregulation of presynaptic proteins and protein kinases associated with enhanced glutamate release from axonal terminals (synaptosomes) of the medial prefrontal cortex in rats with neuropathic pain. Pain 155:377–387.
48. Ishikawa A, Ambroggi F, Nicola SM, Fields HL (2008) Dorsomedial prefrontal cortex contribution to behavioral and nucleus accumbens neuronal responses to incentive cues. J Neurosci 28:5088–5098.
49. Jensen KB, Kosek E, Wicksell R, Kemani M, Olsson G, Merle JV, Kadetoff D, Ingvar M (2012) Cognitive behavioral therapy increases pain-evoked activation of the prefrontal cortex in patients with fibromyalgia. Pain 153:1495–1503.
50. Ji G, Neugebauer V (2011) Pain-related deactivation of medial prefrontal cortical neurons involves mGluR1 and GABA(A) receptors. J Neurophysiol 106:2642–2652.
51. Ji G, Neugebauer V (2012) Modulation of medial prefrontal cortical activity using in vivo recordings and optogenetics. Mol Brain 5:36.
52. Ji G, Neugebauer V (2014) CB1 augments mGluR5 function in medial pre frontal cortical neurons to inhibit amygdala hyperactivity in an arthritis pain model. Eur J Neurosci 39:455–466.
53. Ji G, Sun H, Fu Y, Li Z, Pais-Vieira M, Galhardo V, Neugebauer V (2010) Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation. J Neurosci 30:5451–5464.
54. Johansen JP, Fields HL (2004) Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat Neurosci 7:398–403.
55. Jørum E, Warncke T, Stubhaug A (2003) Cold allodynia and hyperalgesia in neuropathic pain: the effect of N-methyl-D-aspartate (NMDA) receptor antagonist ketamine—a double-blind, cross-over comparison with alfentanil and placebo. Pain 101:229–235.
56. Kalivas PW, Volkow N, Seamans J (2005) Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 45:647–650.
57. Kanju PM, Parameshwaran K, Sims C, Bahr BA, Shonesy BC, Suppiramaniam V (2008) Ampakine CX516 ameliorates functional deficits in AMPA receptors in a hippocampal slice model of protein accumulation. Exp Neurol 214:55–61.
58. Kim H, Chen L, Lim G, Sung B, Wang S, McCabe MF, Rusanescu G, Yang L, Tian Y, Mao J (2012) Brain indoleamine 2,3-dioxygenase contributes to the comorbidity of pain and depression. J Clin Invest 122:2940–2954.
59. King T, Vera-Portocarrero L, Gutierrez T, Vanderah TW, Dussor G, Lai J, Fields HL, Porreca F (2009) Unmasking the tonic-aversive state in neuropathic pain. Nat Neurosci 12:1364–1366.
60. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238.
61. Kucyi A, Moayedi M, Weissman-Fogel I, Goldberg MB, Freeman BV, Tenenbaum HC, Davis KD (2014) Enhanced medial prefrontal-default mode network functional connectivity in chronic pain and its association with pain rumination. J neurosci 34:3969–3975.
62. Lammel S, Ion DI, Roeper J, Malenka RC (2011) Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70:855–862.
63. Le AM, Lee M, Su C, Zou A, Wang J (2014) AMPAkines have novel analgesic properties in rat models of persistent neuropathic and inflammatory pain. Anesthesiology 121:1080–1090.
64. Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, Shim J, Lee K, Collingridge GL, Kaang BK, Zhuo M (2010) Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science 330:1400–1404.
65. Liston C, Chen AC, Zebley BD, Drysdale AT, Gordon R, Leuchter B, Voss HU, Casey BJ, Etkin A, Dubin MJ (2014) Default mode network mechanisms of transcranial magnetic stimulation in depression. Biol Psychiatry 76: 517–526.
66. Magnusson JE, Martin RV (2002) Additional evidence for the involvement of the basal ganglia in formalin-induced nociception: the role of the nucleus accumbens. Brain Res 942:128–132.
67. Mena JD, Selleck RA, Baldo BA (2013) Mu-opioid stimulation in rat prefrontal cortex engages hypothalamic orexin/hypocretin-containing neurons, and reveals dissociable roles of nucleus accumbens and hypothalamus in cortically driven feeding. J Neurosci 33:18540–18552.
68. Metz AE, Yau HJ, Centeno MV, Apkarian AV, Martina M (2009) Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. Proc Natl Acad Sci U S A 106:2423–2428.
69. Miller LR, Cano A (2009) Comorbid chronic pain and depression: who is at risk? J Pain 10:619–627.
70. Moayedi M, Weissman-Fogel I, Crawley AP, Goldberg MB, Freeman BV, Tenenbaum HC, Davis KD (2011) Contribution of chronic pain and neuroticism to abnormal forebrain gray matter in patients with temporomandibular disorder. Neuroimage 55:277–286.
71. Morgan MM, Sohn JH, Liebeskind JC (1989) Stimulation of the periaqueductal gray matter inhibits nociception at the supraspinal as well as spinal level. Brain Res 502:61–66.
72. Morgan MM, Gold MS, Liebeskind JC, Stein C (1991) Periaqueductal gray stimulation produces a spinally mediated, opioid antinociception for the inflamed hindpaw of the rat. Brain Res 545:17–23.
73. Navratilova E, Porreca F (2014) Reward and motivation in pain and pain relief. Nat Neurosci 17:1304–1312.
74. Nelson A, Schneider DM, Takatoh J, Sakurai K, Wang F, Mooney R (2013) A circuit for motor cortical modulation of auditory cortical activity. J Neurosci 33:14342–14353.
75. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169.
76. Obara I, Goulding SP, Hu JH, Klugmann M, Worley PF, Szumlinski KK (2013) Nerve injury-induced changes in Homer/glutamate receptor signaling contribute to the development and maintenance of neuropathic pain. Pain 154:1932–1945.
77. Ohayon MM, Schatzberg AF (2003) Using chronic pain to predict depressive morbidity in the general population. Arch Gen Psychiatry 60:39–47.
78. Ossipov MH, Morimura K, Porreca F (2014) Descending pain modulation and chronification of pain. Curr Opin Support Palliat Care 8:143–151.
79. Pascual-Leone A, Rubio B, Pallardó F, Catalá MD (1996) Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drugresistant depression. Lancet 348:233–237.
80. Porsolt RD, Anton G, Blavet N, Jalfre M (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379–391.
81. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968–971.
82. 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.
83. Reynolds SM, Berridge KC (2008) Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci 11:423–425.
84. Riva-Posse P, Holtzheimer PE, Garlow SJ, Mayberg HS (2013) Practical considerations in the development and refinement of subcallosal cingulate white matter deep brain stimulation for treatment-resistant depression. World Neurosurg 80:S2.e25–34.
85. Romano JM, Turner JA (1985) Chronic pain and depression: does the evidence support a relationship? Psychol Bull 97:18–34.
86. Russo SJ, Nestler EJ(2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14:609–625.
87. Sawamoto N, Honda M, Okada T, Hanakawa T, Kanda M, Fukuyama H, Konishi J, Shibasaki H (2000) Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. J Neurosci 20:7438–7445.
88. Schlaepfer TE, Kosel M, Nemeroff CB (2003) Efficacy of repetitive transcra nial magnetic stimulation (rTMS) in the treatment of affective disorders. Neuropsychopharmacology 28:201–205.
89. Schneider DM, Nelson A, Mooney R (2014) A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513:189–194.
90. Sesack SR, Pickel VM (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320:145–160.
91. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213–242.
92. Shen HW, Gipson CD, Huits M, Kalivas PW (2014) Prelimbic cortex and ventral tegmental area modulate synaptic plasticity differentially in nucleus accumbens during cocaine-reinstated drug seeking. Neuropsychopharmacology 39:1169–1177.
93. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, Quirk GJ (2012) Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 76:804–812.
94. Suzuki T, Amata M, Sakaue G, Nishimura S, Inoue T, Shibata M, Mashimo T (2007) Experimental neuropathy in mice is associated with delayed behavioral changes related to anxiety and depression. Anesth Analg 104: 1570–1577, table of contents.
95. Tucker DM, Antes JR, Stenslie CE, Barnhardt TM (1978) Anxiety and lateral cerebral function. J Abnorm Psychol 87:380–383.
96. Tye KM, Deisseroth K (2012) Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci 13:251–266.
97. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58.
98. Wang J, Goffer Y, Xu D, Tukey DS, Shamir DB, Eberle SE, Zou AH, Blanck TJ, Ziff EB (2011) A single subanesthetic dose of ketamine relieves depression-like behaviors induced by neuropathic pain in rats. Anesthesiology 115:812–821.
99. Witten IB, Steinberg EE, Lee SY, Davidson TJ, Zalocusky KA, Brodsky M, Yizhar O, Cho SL, Gong S, Ramakrishnan C, Stuber GD, Tye KM, Janak PH, Deisseroth K (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72:721–733.
100. Yu LC, Han JS (1990) Habenula as a relay in the descending pathway from nucleus accumbens to periaqueductal grey subserving antinociception. Int J Neurosci 54:245–251.