Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory

Journal of Neuroscience

Volumn 35, Issue 10, 2015, Pages 4190-4202

  Slaker, Megan ^a   Churchill, Lynn ^b   Todd, Ryan P ^a   Blacktop, Jordan M ^a   Zuloaga, Damian G ^c   Raber, Jacob ^c,d   Darling, Rebecca A ^e   Brown, Travis E ^e   Sorg, Barbara A ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e UNIVERSITY OF WYOMING   (United States)

Author keywords

Cocaine; Conditioned place preference; Memory; Perineuronal net

Indexed keywords

COCAINE; PROTEIN C FOS; CHONDROITIN ABC LYASE; DOPAMINE UPTAKE INHIBITOR; N ACETYLGLUCOSAMINE RECEPTOR; NERVE PROTEIN; PLANT LECTIN; WISTERIA LECTIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXTRACELLULAR MATRIX; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MEMORY; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PERINEURONAL NET; PLACE PREFERENCE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; BRAIN INJURY; COMPLICATION; CONFOCAL MICROSCOPY; DRUG EFFECTS; INJURIES; INSTRUMENTAL CONDITIONING; LEARNING; MEMORY DISORDERS; METABOLISM; NERVE CELL NETWORK; PATHOLOGY; PHYSIOLOGY; REINFORCEMENT; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; ASSOCIATION LEARNING; BRAIN INJURIES; CHONDROITIN ABC LYASE; COCAINE; CONDITIONING, OPERANT; DOPAMINE UPTAKE INHIBITORS; EXTINCTION, PSYCHOLOGICAL; MALE; MEMORY DISORDERS; MICROSCOPY, CONFOCAL; NERVE NET; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PLANT LECTINS; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-ACETYLGLUCOSAMINE; TIME FACTORS;

EID: 84924439938     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3592-14.2015     Document Type: Article

References (62)

1. Abel T, Lattal KM (2001) Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11:180–187.
2. Augustine GJ, Kasai H (2007) Bernard Katz, quantal transmitter release and the foundations of presynaptic physiology. J Physiol 578:623–625.
3. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, McMahon SB, Bradbury EJ (2006) Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 26:10856– 10867.
4. Brown TE, Forquer MR, Cocking DL, Jansen HT, Harding JW, Sorg BA (2007) Role of matrix metalloproteinases in the acquisition and recon-solidation of cocaine-induced conditioned place preference. Learn Mem 14:214–223.
5. Bruckner G, Brauer K, Hartig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8:183–200.
6. Campanac E, Hoffman DA (2013) Repeated cocaine exposure increases fast-spiking interneuron excitability in the rat medial prefrontal cortex. J Neurophysiol 109:2781–2792.
7. Chefer VI, Wang R, Shippenberg TS (2011) Basolateral amygdala-driven augmentation of medial prefrontal cortex GABAergic neurotransmission in response to environmental stimuli associated with cocaine administration. Neuropsychopharmacology 36:2018–2029.
8. Childress AR, Mozley PD, McElgin W, Fitzgerald J, Reivich M, O’Brien CP (1999) Limbic activation during cue-induced cocaine craving. Am J Psychiatry 156:11–18.
9. Ciccocioppo R, Sanna PP, Weiss F (2001) Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D1 antagonists. Proc Natl Acad Sci U S A 98:1976–1981.
10. Corvetti L, Rossi F (2005) Degradation of chondroitin sulfate proteoglycans induces sprouting of intact Purkinje axons in the cerebellum of the adult rat. JNeurosci 25:7150–7158.
11. Costa E, Davis JM, Dong E, Grayson DR, Guidotti A, Tremolizzo L, Veldic M (2004) A GABAergic cortical deficit dominates schizophrenia patho physiology. Crit Rev Neurobiol 16:1–23.
12. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuro-sci Biobehav Rev 28:771–784.
13. Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors: implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277:43707–43716.
14. De Ridder D, Vanneste S, Kovacs S, Sunaert S, Dom G (2011) Transient alcohol craving suppression by rTMS of dorsal anterior cingulate: an fMRI and LORETA EEG study. Neurosci Lett 496:5–10.
15. Dilgen JE, Tompa T, Saggu S, Naselaris T, Lavin A (2013) Optogenetically evoked gamma oscillations are disturbed by cocaine administration. Front Cell Neurosci 7:213.
16. Dityatev A, Bruckner G, Dityateva G, Grosche J, Kleene R, Schachner M (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 67: 570–588.
17. Dong Y, Nasif FJ, Tsui JJ, Ju WY, Cooper DC, Hu XT, Malenka RC, White FJ (2005) Cocaine-induced plasticity of intrinsic membrane properties in prefrontal cortex pyramidal neurons: adaptations in potassium currents. J Neurosci 25:936-940.
18. Ford KA, Wolf ME, Hu XT (2009) Plasticity of L-type Ca2+ channels after cocaine withdrawal. Synapse 63:690–697.
19. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12:897–904.
20. Fuchs RA, Evans KA, Ledford CC, Parker MP, Case JM, Mehta RH, See RE (2005) The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30:296–309.
21. Gherardini L, Gennaro M, Pizzorusso T (2015) Perilesional treatment with chondroitinase ABC and motor training promote functional recovery after stroke in rats. Cereb Cortex 25:202–212.
22. Gogolla N, Caroni P, Lüthi A, Herry C (2009) Perineuronal nets protect fear memories from erasure. Science 325:1258–1261.
23. Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652–669.
24. Grant S, London ED, Newlin DB, Villemagne VL, Liu X, Contoreggi C, Phil- lips RL, Kimes AS, Margolin A (1996) Activation of memory circuits during cue-elicited cocaine craving. Proc Natl Acad Sci U S A 93:12040–12045.
25. Happel MF, Niekisch H, Castiblanco Rivera LL, Ohl FW, Deliano M, Frisch-knecht R (2014) Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex. Proc Natl Acad Sci U S A 111:2800–2805.
26. Härtig W, Brauer K, Brückner G (1992) Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport 3:869–872.
27. Hearing M, Kotecki L, Marron Fernandez de Velasco E, Fajardo-Serrano A, Chung HJ, Luján R, Wickman K (2013) Repeated cocaine weakens GABA(B)-Girk signaling in layer 5/6 pyramidal neurons in the prelimbic cortex. Neuron 80:159–170.
28. Heinrichs SC, Leite-Morris KA, Carey RJ, Kaplan GB (2010) Baclofen enhances extinctionofopiate conditioned place preference. Behav Brain Res 207:353–359.
29. Huang CC, Lin HJ, Hsu KS (2007a) Repeated cocaine administration promotes long-term potentiation induction in rat medial prefrontal cortex. Cereb Cortex 17:1877–1888.
30. Huang CC, Yang PC, Lin HJ, Hsu KS (2007b) Repeated cocaine administration impairs group II metabotropic glutamate receptor-mediated long-term depressioninrat medial prefrontal cortex. JNeurosci 27:2958–2968.
31. Hylin MJ, Orsi SA, Moore AN, Dash PK (2013) Disruption of the perineu-ronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning. Learn Mem 20:267–273.
32. Itzhak Y, Anderson KL (2012) Changes in the magnitude of drug-unconditioned stimulus during conditioning modulate cocaine-induced place preference in mice. Addict Biol 17:706–716.
33. Jayaram P, Steketee JD (2005) Effects of cocaine-induced behavioural sen-sitization on GABA transmission within rat medial prefrontal cortex. Eur J Neurosci 21:2035–2039.
34. Jentsch JD, Taylor JR (1999) Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology 146:373–390.
35. Kalivas PW, McFarland K (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology 168:44–56.
36. Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413.
37. Kilts CD, Schweitzer JB, Quinn CK, Gross RE, Faber TL, Muhammad F, Ely TD, Hoffman JM, Drexler KP (2001) Neural activity related to drug craving in cocaine addiction. Arch Gen Psychiatry 58:334–341.
38. LaLumiere RT, Niehoff KE, Kalivas PW (2010) The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learn Mem 17:168–175.
39. Lee JL (2010) Memory reconsolidation mediates the updatingof hippocam-pal memory content. Front Behav Neurosci 4:168.
40. Maas LC, Lukas SE, Kaufman MJ, Weiss RD, Daniels SL, Rogers VW, Kukes TJ, Renshaw PF (1998) Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. Am J Psychiatry 155:124–126.
41. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neu-rosci 5:793–807.
42. Mauney SA, Athanas KM, Pantazopoulos H, Shaskan N, Passeri E, Berretta S, Woo TU (2013) Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biol Psychiatry 74:427–435.
43. McFarland K, Kalivas PW (2001) The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 21:8655–8663.
44. Miller CA, Marshall JF (2004) Altered prelimbic cortex output during cue-elicited drug seeking. J Neurosci 24:6889–6897.
45. Nasif FJ, Hu XT, White FJ (2005a) Repeated cocaine administration increases voltage-sensitive calcium currents in response to membrane depolarization in medial prefrontal cortex pyramidal neurons. J Neurosci 25:3674–3679.
46. Nasif FJ, Sidiropoulou K, Hu XT, White FJ (2005b) Repeated cocaine administration increases membrane excitabilityof pyramidal neuronsin the rat medial prefrontal cortex. J Pharmacol Exp Ther 312:1305–1313.
47. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Amsterdam: Elsevier.
48. Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16:279–288.
49. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251.
50. Robbins TW, Ersche KD, Everitt BJ (2008) Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141:1–21.
51. Robinson MJ, Franklin KB (2010) Reconsolidation of a morphine place preference: impact of the strength and age of memory on disruption by propranolol and midazolam. Behav Brain Res 213:201–207.
52. Robinson MJ, Armson M, Franklin KB (2011) The effect ofpropranolol and midazolam on the reconsolidation of a morphine place preference in chronically treated rats. Front Behav Neurosci 5:42.
53. Rudy JW, Biedenkapp JC, O’Reilly RC (2005) Prefrontal cortex and the organization of recent and remote memories: an alternative view. Learn Mem 12:445–446.
54. Schüppel K, Brauer K, Härtig W, Grosche J, Earley B, Leonard BE, Brückner G (2002) Perineuronal nets of extracellular matrix around hippocampal interneurons resist destruction by activated microglia in trimethyltin-treated rats. Brain Res 958:448–453.
55. Sparta DR, Hovelsø N, Mason AO, Kantak PA, Ung RL, Decot HK, Stuber GD (2014) Activation of prefrontal cortical parvalbumin interneurons facilitates extinction of reward-seeking behavior. J Neurosci 34:3699–3705.
56. Stefanik MT, Moussawi K, Kupchik YM, Smith KC, Miller RL, Huff ML, Deisseroth K, Kalivas PW, LaLumiere RT (2013) Optogenetic inhibition of cocaine seeking in rats. Addict Biol 18:50–53.
57. Steullet P, Cabungcal JH, Cuénod M, Do KQ (2014) Fast oscillatory activity in the anterior cingulate cortex: dopaminergic modulation and effect of perineuronal net loss. Front Cell Neurosci 8:244.
58. Sun W, Rebec GV (2006) Repeated cocaine self-administration alters processing of cocaine-related informationinrat prefrontal cortex. J Neurosci 26:8004–8008.
59. Tsien RY (2013) Very long-term memories may be stored in the pattern of holes inthe perineuronal net. Proc Natl Acad SciU S A110:12456–12461.
60. VandenOever MC, Lubbers BR, Goriounova NA, LiK W, Van derSchors RC, Loos M, Riga D, Wiskerke J, Binnekade R, Stegeman M, Schoffelmeer AN, Mansvelder HD, Smit AB, De Vries TJ, Spijker S (2010) Extracellular matrix plasticity and GABAergic inhibition of prefrontal cortex pyramidal cells facilitates relapse to heroin seeking. Neuropsychopharmacology 35:2120–2133.
61. Xue YX, Xue LF, Liu JF, He J, Deng JH, Sun SC, Han HB, Luo YX, Xu LZ, Wu P, Lu L (2014) Depletion of perineuronal nets in the amygdala to enhance the erasure of drug memories. J Neurosci 34:6647–6658.
62. Zhao RR, Fawcett JW (2013) Combination treatment with chondroitinase ABC in spinal cord injury-breaking the barrier. Neurosci Bull 29:477– 483.