A cholinergic-dependent role for the entorhinal cortex in trace fear conditioning

Journal of Neuroscience

Volumn 29, Issue 25, 2009, Pages 8087-8093

  Esclassan, Frederic ^a,b,c   Coutureau, Etienne ^a,b   Di Scala, Georges ^a,b   Marchand, Alain R ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c Université Paul Sabatier   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; IMMUNOGLOBULIN G; MUSCARINIC M1 RECEPTOR; MUSCARINIC RECEPTOR; PIRENZEPINE; SAPORIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC ACTIVITY; CONDITIONING; CONTROLLED STUDY; DOSE RESPONSE; ENTORHINAL CORTEX; EXPERIMENTAL RAT; FEAR; FREEZING; INTERNEURON; MALE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE;

ACETYLCHOLINE; ACOUSTIC STIMULATION; ANIMALS; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROSHOCK; ENTORHINAL CORTEX; EXCITATORY AMINO ACID AGONISTS; FEAR; IMMUNOHISTOCHEMISTRY; IMMUNOTOXINS; MALE; MICROINJECTIONS; MUSCARINIC ANTAGONISTS; N-METHYLASPARTATE; PIRENZEPINE; RATS; RATS, LONG-EVANS; REACTION TIME; RECEPTOR, MUSCARINIC M1; RIBOSOME INACTIVATING PROTEINS, TYPE 1; STARTLE REACTION;

EID: 67649382232     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0543-09.2009     Document Type: Article

References (62)

1. Acquas E, Wilson C, Fibiger HC (1996) Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J Neurosci 16:3089-3096. (Pubitemid 26121851)
2. Baldi E, Ambrogi Lorenzini C, Sacchetti B, Tassoni G, Bucherelli C (1998) Entorhinal cortex and fimbria-fornix role in rat's passive avoidance response memorization. Brain Res 799:270-277. (Pubitemid 28351257)
3. Bangasser DA, Waxler DE, Santollo J, Shors TJ (2006) Trace conditioning and the hippocampus: the importance of contiguity. J Neurosci 26:8702-8706. (Pubitemid 44319405)
4. Bayraktar T, Staiger JF, Acsady L, Cozzari C, Freund TF, Zilles K (1997) Co-localization of vasoactive intestinal polypeptide, gammaaminobutyric acid and choline acetyltransferase in neocortical interneurons of the adult rat. Brain Res 757:209-217. (Pubitemid 27244599)
5. Bocian R, Konopacki J (2004) The effect of posterior hypothalamic injection of cholinergic agents on hippocampal formation theta in freely moving cat. Brain Res Bull 63:283-294. (Pubitemid 38758038)
6. Bruno JP, Gash C, Martin B, Zmarowski A, Pomerleau F, Burmeister J, Huettl P, Gerhardt GA (2006) Second-by-second measurement of acetylcholine release in prefrontal cortex. Eur J Neurosci 24:2749-2757. (Pubitemid 44813826)
7. Carter RM, Hofstotter C, Tsuchiya N, Koch C (2003) Working memory and fear conditioning. Proc Natl Acad Sci U S A 100:1399-1404. (Pubitemid 36184013)
8. Carter RM, O'Doherty JP, Seymour B, Koch C, Dolan RJ (2006) Contingency awareness in human aversive conditioning involves the middle frontal gyrus. Neuroimage 29:1007-1012. (Pubitemid 43121224)
9. Chedotal A, Cozzari C, Faure MP, Hartman BK, Hamel E (1994) Distinct choline acetyltransferase (ChAT) and vasoactive intestinal polypeptide (VIP) bipolar neurons project to local blood vessels in the rat cerebral cortex. Brain Res 646:181-193. (Pubitemid 24151750)
10. Chowdhury N, Quinn JJ, Fanselow MS (2005) Dorsal hippocampus involvement in trace fear conditioning with long, but not short, trace intervals in mice. Behav Neurosci 119:1396-1402. (Pubitemid 41598752)
11. Chudasama Y, Dalley JW, Nathwani F, Bouger P, Robbins TW (2004) Cholinergic modulation of visual attention and working memory: dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learn Mem 11:78-86. (Pubitemid 38167061)
12. Clark RE, Squire LR (1998) Classical conditioning and brain systems: the role of awareness. Science 280:77-81. (Pubitemid 28169083)
13. Clark RE, Manns JR, Squire LR (2002) Classical conditioning, awareness, and brain systems. Trends Cogn Sci 6:524-531. (Pubitemid 35430391)
14. Coutureau E, Galani R, Gosselin O, Majchrzak M, Di Scala G (1999) Entorhinal but not hippocampal or subicular lesions disrupt latent inhibition in rats. Neurobiol Learn Mem 72:143-157.
15. Coutureau E, Killcross AS, Good M, Marshall VJ, Ward-Robinson J, Honey RC (2002) Acquired equivalence and distinctiveness of cues: II. Neural manipulations and their implications. J Exp Psychol Anim Behav Process 28:388-396. (Pubitemid 44220035)
16. de Lacalle S, Kulkarni S, Wiley RG (1998) Lesion-induced transneuronal plasticity of the cholinergic innervation in the adult rat entorhinal cortex. Eur J Neurosci 10:1054-1062. (Pubitemid 28375630)
17. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178. (Pubitemid 35340120)
18. Esclassan F, Coutureau E, Di Scala G, Marchand AR (2009) Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 19:33-44.
19. Gaykema RP, Luiten PG, Nyakas C, Traber J (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103-124. (Pubitemid 20092475)
20. Gilmartin MR, McEchron MD (2005) Single neurons in the dentate gyrus and CA1 of the hippocampus exhibit inverse patterns of encoding during trace fear conditioning. Behav Neurosci 119:164-179. (Pubitemid 40279507)
21. Gormezano I, Kehoe EJ, Marshall BS (1983) Twenty years of classical conditioning research with the rabbit. Prog Psychobiol Physiol Psychol 10:197-275.
22. Grossberg S, Merrill JW (1992) A neural network model of adaptively timed reinforcement learning and hippocampal dynamics. Brain Res Cogn Brain Res 1:3-38.
23. Gutiérrez H, Gutiérrez R, Silva-Gandarias R, Estrada J, Miranda MI, Bermúdez-Rattoni F (1999) Differential effects of 192IgG-saporin and NMDA-induced lesions into the basal forebrain on cholinergic activity and taste aversion memory formation. Brain Res 834:136-141. (Pubitemid 29332018)
24. Han CJ, O'Tuathaigh CM, van Trigt L, Quinn JJ, Fanselow MS, Mongeau R, Koch C, Anderson DJ (2003) Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proc Natl Acad Sci U S A 100:13087-13092. (Pubitemid 37340030)
25. Hasselmo ME, Stern CE (2006) Mechanisms underlying working memory for novel information. Trends Cogn Sci 10:487-493. (Pubitemid 44602572)
26. Hasselmo ME, Giocomo LM, Zilli EA (2007) Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17:1252-1271. (Pubitemid 350244240)
27. Holland PC (2008) Cognitive versus stimulus-response theories of learning. Learn Behav 36:227-241.
28. Hunt PS, Richardson R (2007) Pharmacological dissociation of trace and long-delay fear conditioning in young rats. Neurobiol Learn Mem 87:86-92. (Pubitemid 44667573)
29. Hunt PS, Barnet RC, Shea ME, Baker EM (2006) Cholinergic modulation of trace conditioning trained in serial compound: a developmental analysis. Neurobiol Learn Mem 86:311-321. (Pubitemid 44436976)
30. Izquierdo I, Quillfeldt JA, Zanatta MS, Quevedo J, Schaeffer E, Schmitz PK, Medina JH (1997) Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur J Neurosci 9:786-793. (Pubitemid 27190088)
31. Kaneko T, Thompson RF (1997) Disruption of trace conditioning of the nictitating membrane response in rabbits by central cholinergic blockade. Psychopharmacology (Berl) 131:161-166. (Pubitemid 27261604)
32. Kerr KM, Agster KL, Furtak SC, Burwell RD (2007) Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 17:697-708. (Pubitemid 47493452)
33. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184. (Pubitemid 30350041)
34. Levey AI, Kitt CA, Simonds WF, Price DL, Brann MR (1991) Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 11:3218-3226.
35. Levy WB, Sanyal A, Rodriguez P, Sullivan DW, Wu XB (2005) The formation of neural codes in the hippocampus: trace conditioning as a prototypical paradigm for studying the random recoding hypothesis. Biol Cybern 92:409-426. (Pubitemid 40834170)
36. Lewis MC, Gould TJ (2007) Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice. Hippocampus 17:462-470. (Pubitemid 46897979)
37. Marchand AR, Kamper E (2000) Time course of cardiac conditioned responses in restrained rats as a function of the trace CS-US interval. J Exp Psychol Anim Behav Process 26:385-398.
38. Marchand AR, Luck D, DiScala G (2003) Evaluation of an improved automated analysis of freezing behaviour in rats and its use in trace fear conditioning. J Neurosci Methods 126:145-153. (Pubitemid 36694155)
39. Marques Pereira P, Cosquer B, Schimchowitsch S, Cassel JC (2005) Hebb-Williams performance and scopolamine challenge in rats with partial immunotoxic hippocampal cholinergic deafferentation. Brain Res Bull 64:381-394. (Pubitemid 39656118)
40. McAlonan GM, Wilkinson LS, Robbins TW, Everitt BJ (1995) The effects of AMPA-induced lesions of the septo-hippocampal cholinergic projection on aversive conditioning to explicit and contextual cues and spatial learning in the water maze. Eur J Neurosci 7:281-292.
41. McEchron MD, Bouwmeester H, Tseng W, Weiss C, Disterhoft JF (1998) Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8:638-646. (Pubitemid 29010191)
42. McGaughy J, Koene RA, Eichenbaum H, Hasselmo ME (2005) Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. J Neurosci 25:10273-10281. (Pubitemid 41636224)
43. Misane I, Tovote P, Meyer M, Spiess J, Ogren SO, Stiedl O (2005) Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 15:418-426. (Pubitemid 40916289)
44. Ohtake T, Heckers S, Wiley RG, Lappi DA, Mesulam MM, Geula C (1997) Retrograde degeneration and colchicine protection of basal forebrain cholinergic neurons following hippocampal injections of an immunotoxin against the P75 nerve growth factor receptor. Neuroscience 78:123-133. (Pubitemid 27132590)
45. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. New York: Academic.
46. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
47. Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369-391. (Pubitemid 30462094)
48. Quinn JJ, Oommen SS, Morrison GE, Fanselow MS (2002) Post-training excitotoxic lesions of the dorsal hippocampus attenuate forward trace, backward trace, and delay fear conditioning in a temporally specific manner. Hippocampus 12:495-504. (Pubitemid 34906478)
49. Ryou JW, Cho SY, Kim HT (2001) Lesions of the entorhinal cortex impair acquisition of hippocampal-dependent trace conditioning. Neurobiol Learn Mem 75:121-127. (Pubitemid 34127513)
50. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758-762.
51. Seager MA, Asaka Y, Berry SD (1999) Scopolamine disruption of behavioral and hippocampal responses in appetitive trace classical conditioning. Behav Brain Res 100:143-151. (Pubitemid 29130248)
52. Selden NR, Everitt BJ, Jarrard LE, Robbins TW (1991) Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 42:335-350.
53. Shohamy D, Allen MT, Gluck MA (2000) Dissociating entorhinal and hippocampal involvement in latent inhibition. Behav Neurosci 114:867-874. (Pubitemid 30796096)
54. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100:729-744. (Pubitemid 17208210)
55. Tahvildari B, Fransén E, Alonso AA, Hasselmo ME (2007) Switching between "On" and "Off" states of persistent activity in lateral entorhinal layer III neurons. Hippocampus 17:257-263.
56. Talnov AN, Quian Quiroga R, Meier M, Matsumoto G, Brankack J (2003) Entorhinal inputs to dentate gyrus are activated mainly by conditioned events with long time intervals. Hippocampus 13:755-765. (Pubitemid 37098762)
57. Tang Y, Mishkin M, Aigner TG (1997) Effects of muscarinic blockade in perirhinal cortex during visual recognition. Proc Natl Acad Sci U S A 94:12667-12669. (Pubitemid 27492586)
58. Totterdell S, Meredith GE (1997) Topographical organization of projections from the entorhinal cortex to the striatum of the rat. Neurosci 78:715-729. (Pubitemid 27179654)
59. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578-598. (Pubitemid 33103727)
60. Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21:317-323. (Pubitemid 28341955)
61. Yoon T, Otto T (2007) Differential contributions of dorsal vs. ventral hippocampus to auditory trace fear conditioning. Neurobiol Learn Mem 87:464-475. (Pubitemid 46483128)
62. Yoshida M, FranséE, Hasselmo ME (2008) mGluR-dependent persistent firing in entorhinal cortex layer III neurons. Eur J Neurosci 28:1116-1126.