Choice behavior guided by learned, but not innate, taste aversion recruits the orbitofrontal cortex

Journal of Neuroscience

Volumn 36, Issue 41, 2016, Pages 10574-10583

  Ramírez Lugo, Leticia ^a   Peñas Rincón, Ana ^a   Ángeles Durán, Sandybel ^a   Sotres Bayon, Francisco ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Conditioning; Decision; Gustatory; Inactivation; Insular; Prefontal

Indexed keywords

PROTEIN C FOS; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; MUSCIMOL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECISION MAKING; FLUID INTAKE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INSULA; LEARNING; MALE; MOTIVATION; NONHUMAN; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STIMULUS; TASK PERFORMANCE; TASTE AVERSION; WORKING MEMORY; ANIMAL; AVOIDANCE BEHAVIOR; DRUG EFFECTS; MEMORY; METABOLISM; PHYSIOLOGY; TASTE; WISTAR RAT;

ANIMALS; AVOIDANCE LEARNING; CHOICE BEHAVIOR; GABA AGONISTS; LEARNING; MALE; MEMORY; MUSCIMOL; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GABA-B; TASTE; TASTE PERCEPTION;

EID: 84991461426     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0796-16.2016     Document Type: Article

References (56)

1. Akirav I, Khatsrinov V, Vouimba RM, Merhav M, Ferreira G, Rosenblum K, Maroun M (2006) Extinction of conditioned taste aversion depends on functional protein synthesis but not on NMDA receptor activation in the ventromedial prefrontal cortex. Learn Mem 13:254–258.
2. Balleine BW, Leung BK, Ostlund SB (2011) The orbitofrontal cortex, predicted value, and choice. Ann N Y Acad Sci 1239:43–50.
3. Berman DE, Hazvi S, Neduva V, Dudai Y (2000) The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: activation of ERK1–2 and formation of a memory trace. J Neurosci 20: 7017–7023.
4. Bermúdez-Rattoni F (2004) Molecular mechanisms of taste-recognition memory. Nat Rev Neurosci 5:209–217.
5. Bermúdez-Rattoni F, Introini-Collison I, Coleman-Mesches K, McGaugh JL (1997) Insular cortex and amygdala lesions induced after aversive training impair retention: effects of degree of training. Neurobiol Learn Mem 67:57–63.
6. 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.
7. Bravo-Rivera C, Roman-Ortiz C, Brignoni-Perez E, Sotres-Bayon F, Quirk GJ (2014) Neural structures mediating expression and extinction of platformmediated avoidance. J Neurosci 34:9736–9742.
8. Bures J, Bermúdez-Rattoni F, Yamamoto T (1998) Conditioned taste aversion: memory of a special kind. Oxford: OUP.
9. 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.
10. Elliott R, Agnew Z, Deakin JF (2008) Medial orbitofrontal cortex codes relative rather than absolute value of financial rewards in humans. Eur J Neurosci 27:2213–2218.
11. Gallagher M, McMahan RW, Schoenbaum G (1999) Orbitofrontal cortex and representation of incentive value in associative learning. J Neurosci 19:6610–6614.
12. Gallo M, Roldan G, Bures J (1992) Differential involvement of gustatory insular cortex and amygdala in the acquisition and retrieval of conditioned taste aversion in rats. Behav Brain Res 52:91–97.
13. Gonzalez MC, Villar ME, Igaz LM, Viola H, Medina JH (2015) Dorsal medial prefrontal cortex contributes to conditioned taste aversion memory consolidation and retrieval. Neurobiol Learn Mem 126:1–6.
14. Grabenhorst F, Rolls ET (2009) Different representations of relative and absolute subjective value in the human brain. Neuroimage 48:258–268.
15. Hernádi I, Karádi Z, Vígh J, Petykó Z, Egyed R, Berta B, Lénárd L (2000) Alterations of conditioned taste aversion after microiontophoretically applied neurotoxins in the medial prefrontal cortex of the rat. Brain Res Bull 53:751–758.
16. Holmes NM, Marchand AR, Coutureau E (2010) Pavlovian to instrumental transfer: a neurobehavioural perspective. Neurosci Biobehav Rev 34: 1277–1295.
17. Hoover WB, Vertes RP (2011) Projections of the medial orbital and ventral orbital cortex in the rat. J Comp Neurol 519:3766–3801.
18. Ishii H, Ohara S, Tobler PN, Tsutsui K, Iijima T (2012) Inactivating anterior insular cortex reduces risk taking. J Neurosci 32:16031–16039.
19. Jezzini A, Mazzucato L, La Camera G, Fontanini A (2013) Processing of hedonic and chemosensory features of taste in medial prefrontal and insular networks. J Neurosci 33:18966–18978.
20. King CT, Hashimoto K, Blonde GD, Spector AC (2015) Unconditioned oromotor taste reactivity elicited by sucrose and quinine is unaffected by extensive bilateral damage to the gustatory zone of the insular cortex in rats. Brain Res 1599:9–19.
21. Knapska E, Maren S (2009) Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn Mem 16:486–493.
22. Lara AH, Kennerley SW, Wallis JD (2009) Encoding of gustatory working memory by orbitofrontal neurons. J Neurosci 29:765–774.
23. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155–184.
24. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069.
25. Lin PY, Wang SP, Tai MY, Tsai YF (2010) Differential involvement of medial prefrontal cortex and basolateral amygdala extracellular signalregulated kinase in extinction of conditioned taste aversion is dependent on different intervals of extinction following conditioning. Neuroscience 171:125–133.
26. MacDonald CJ, Meck WH, Simon SA, Nicolelis MA (2009) Taste-guided decisions differentially engage neuronal ensembles across gustatory cortices. J Neurosci 29:11271–11282.
27. Machado CJ, Bachevalier J (2007) The effects of selective amygdala, orbital frontal cortex or hippocampal formation lesions on reward assessment in nonhuman primates. Eur J Neurosci 25:2885–2904.
28. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844–852.
29. Marotta R, Fenu S, Scheggi S, Vinci S, Rosas M, Falqui A, Gambarana C, De Montis MG, Acquas E (2014) Acquisition and expression of conditioned taste aversion differentially affects extracellular signal regulated kinase and glutamate receptor phosphorylation in rat prefrontal cortex and nucleus accumbens. Front Behav Neurosci 8:153.
30. Mickley GA, Kenmuir CL, Yocom AM, Wellman JA, Biada JM (2005) A role for prefrontal cortex in the extinction of a conditioned taste aversion. Brain Res 1051:176–182.
31. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70–74.
32. Namburi P, Al-Hasani R, Calhoon GG, Bruchas MR, Tye KM (2016) Architectural representation of valence in the limbic system. Neuropsychopharmacology 41:1697–1715.
33. Ostlund SB, Balleine BW (2007) The contribution of orbitofrontal cortex to action selection. Ann N Y Acad Sci 1121:174–192.
34. Padoa-Schioppa C, Assad JA (2008) The representation of economic value in the orbitofrontal cortex is invariant for changes of menu. Nat Neurosci 11:95–102.
35. Parkes SL, Balleine BW (2013) Incentive memory: evidence the basolateral amygdala encodes and the insular cortex retrieves outcome values to guide choice between goal-directed actions. J Neurosci 33:8753–8763.
36. Paulus MP (2007) Decision-making dysfunctions in psychiatry–altered homeostatic processing? Science 318:602–606.
37. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
38. Pickens CL, Saddoris MP, Setlow B, Gallagher M, Holland PC, Schoenbaum G (2003) Different roles for orbitofrontal cortex and basolateral amygdala in a reinforcer devaluation task. J Neurosci 23:11078–11084.
39. Pickens CL, Saddoris MP, Gallagher M, Holland PC (2005) Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task. Behav Neurosci 119:317–322.
40. Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54–71.
41. Quirk GJ, Armony JL, LeDoux JE (1997) Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19:613–624.
42. Rangel A, Camerer C, Montague PR (2008) A framework for studying the neurobiology of value-based decision making. Nat Rev Neurosci 9:545– 556.
43. Rich EL, Wallis JD (2014) Medial-lateral organization of the orbitofrontal cortex. J Cogn Neurosci 26:1347–1362.
44. Rich EL, Wallis JD (2016) Decoding subjective decisions from orbitofrontal cortex. Nat Neurosci 19:973–980.
45. Rolls ET (2004) The functions of the orbitofrontal cortex. Brain Cogn 55: 11–29.
46. Schoenbaum G, Roesch M (2005) Orbitofrontal cortex, associative learning, and expectancies. Neuron 47:633–636.
47. Schoenbaum G, Setlow B (2001) Integrating orbitofrontal cortex into prefrontal theory: common processing themes across species and subdivisions. Learn Mem 8:134–147.
48. Schoenbaum G, Takahashi Y, Liu TL, McDannald MA (2011) Doestheorbitofrontal cortex signal value? Ann N Y Acad Sci 1239:87–99.
49. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–538.
50. Sotres-Bayon F, Quirk GJ (2010) Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol 20:231–235.
51. Sotres-Bayon F, Diaz-Mataix L, Bush DE, LeDoux JE (2009) Dissociable roles for the ventromedial prefrontal cortex and amygdala in fear extinction: NR2B contribution. Cereb Cortex 19:474–482.
52. Stalnaker TA, Cooch NK, Schoenbaum G (2015) What the orbitofrontal cortex does not do. Nat Neurosci 18:620–627.
53. Sugrue LP, Corrado GS, Newsome WT (2005) Choosing the greater of two goods: neural currencies for valuation and decision making. Nat Rev Neurosci 6:363–375.
54. Tremblay L, Schultz W (1999) Relative reward preference in primate orbitofrontal cortex. Nature 398:704–708.
55. Wallis JD (2012) Cross-species studies of orbitofrontal cortex and valuebased decision-making. Nat Neurosci 15:13–19.
56. Xin J, Ma L, Zhang TY, Yu H, Wang Y, Kong L, Chen ZY (2014) Involvement of BDNF signaling transmission from basolateral amygdala to infralimbic prefrontal cortex in conditioned taste aversion extinction. J Neurosci 34:7302–7313.