Predicting aversive events and terminating fear in the mouse anterior cingulate cortex during trace fear conditioning

Journal of Neuroscience

Volumn 32, Issue 3, 2012, Pages 1082-1095

  Steenland, Hendrik W ^a   Li, Xiang Yao ^a,c   Zhuo, Min ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b Seoul National University   (South Korea)

^c XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; CONDITIONING; ELECTRIC POTENTIAL; ELECTROMYOGRAM; EVOKED RESPONSE; FEAR; FREEZING; HISTOLOGY; LEARNING; MALE; MEMORY; MOTOR ACTIVITY; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SINGLE UNIT ACTIVITY; SPIKE WAVE; TRACE FEAR CONDITIONING;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; EVOKED POTENTIALS; EXPLORATORY BEHAVIOR; FEAR; FOURIER ANALYSIS; FREEZING REACTION, CATALEPTIC; GYRUS CINGULI; MALE; MICE; MICE, INBRED C57BL; PYRAMIDAL CELLS;

EID: 84862946406     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5566-11.2012     Document Type: Article

References (47)

1. Baeg EH, Kim YB, Jang J, Kim HT, Mook-Jung I, Jung MW (2001) Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of the rat. Cereb Cortex 11:441-451.
2. Bancaud J, Talairach J, Geier S, Bonis A, Trottier S, Manrique M (1976) Behavioral manifestations induced by electric stimulation of the anterior cingulate gyrus in man. Rev Neurol (Paris) 132:705-724.
3. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G (2004) Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92:600-608.
4. Bissiére 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.
5. Büchel C, Morris J, Dolan RJ, Friston KJ (1998) Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20:947-957.
6. Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279-306.
7. Ding HK, Teixeira CM, Frankland PW (2008) Inactivation of the anterior cingulate cortex blocks expression of remote, but not recent, conditioned taste aversion memory. Learn Mem 15:290-293.
8. Dum RP, Levinthal DJ, Strick PL (2009) The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 29:14223-14235.
9. Freeman JH Jr, Cuppernell C, Flannery K, Gabriel M (1996) Limbic thalamic, cingulate cortical and hippocampal neuronal correlates of discriminative approach learning in rabbits. Behav Brain Res 80:123-136.
10. Gabriel M, Vogt BA, Kubota Y, Poremba A, Kang E (1991a) Training-stage related neuronal plasticity in limbic thalamus and cingulate cortex during learning: a possible key to mnemonic retrieval. Behav Brain Res 46:175-185.
11. Gabriel M, Kubota Y, Sparenborg S, Straube K, Vogt BA (1991b) Effects of cingulate cortical lesions on avoidance learning and training-induced unit activity in rabbits. Exp Brain Res 86:585-600.
12. Gilmartin MR, Helmstetter FJ (2010) Trace and contextual fear conditioning require neural activity and NMDA receptor-dependent transmission in the medial prefrontal cortex. Learn Mem 17:289-296.
13. Gilmartin MR, McEchron MD (2005) Single neurons in the medial prefrontal cortex of the rat exhibit tonic and phasic coding during trace fear conditioning. Behav Neurosci 119:1496-1510.
14. 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.
15. Huerta PT, Sun LD, Wilson MA, Tonegawa S (2000) Formation of temporalmemory requiresNMDAreceptors within CA1 pyramidal neurons. Neuron 25:473-480.
16. Hughes JR, Mazurowski JA (1962) Studies on the supracallosal mesial cortex of unanesthetized, conscious mammals. II. Monkey. A. Movements elicited by electrical stimulation. Electroencephalogr Clin Neurophysiol 14:477-485.
17. Jeantet Y, Cho YH (2003) Design of a twin tetrode microdrive and headstage for hippocampal single unit recordings in behaving mice. J Neurosci Methods 129:129-134.
18. Johansen JP, Fields HL (2004) Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat Neurosci 7:398-403.
19. Jürgens U (2009) The neural control of vocalization in mammals: a review. J Voice 23:1-10.
20. Jürgens U, Pratt R (1979) The cingular vocalization pathway in the squirrel monkey. Exp Brain Res 34:499-510.
21. Knight DC, Cheng DT, Smith CN, Stein EA, Helmstetter FJ (2004) Neural substrates mediating human delay and trace fear conditioning. J Neurosci 24:218-228.
22. Koyama T, Tanaka YZ, Mikami A (1998) Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain. Neuroreport 9:2663-2667.
23. Koyama T, Kato K, Mikami A (2000) During pain-avoidance neurons activated in the macaque anterior cingulate and caudate. Neurosci Lett 283:17-20.
24. Koyama T, Kato K, Tanaka YZ, Mikami A (2001) Anterior cingulate activity during pain-avoidance and reward tasks in monkeys. Neurosci Res 39:421-430.
25. Kubota Y, Wolske M, Poremba A, Kang E, Gabriel M (1996) Stimulusrelated and movement-related single-unit activity in rabbit cingulate cortex and limbic thalamus during performance of discriminative avoidance behavior. Brain Res 721:22-38.
26. Kuo CC, Yen CT (2005) Comparison of anterior cingulate and primary somatosensory neuronal responses to noxious laser-heat stimuli in conscious, behaving rats. J Neurophysiol 94:1825-1836.
27. Mears RP, Boutros NN, Cromwell HC (2009) Reduction of prelimbic inhibitory gating of auditory evoked potentials after fear conditioning. Behav Neurosci 123:315-327.
28. Narayanan RT, Seidenbecher T, Kluge C, Bergado J, Stork O, Pape HC (2007) Dissociated theta phase synchronization in amygdalo-hippocampal circuits during various stages of fear memory. Eur J Neurosci 25:1823-1831.
29. Nili U, Goldberg H, Weizman A, Dudai Y (2010) Fear thou not: activity of frontal and temporal circuits in moments of real-life courage. Neuron 66:949-962.
30. Paré D, Collins DR (2000) Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J Neurosci 20:2701-2710.
31. Paxinos G, Franklin K (2003) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
32. Paz R, Bauer EP, Paré D (2008) Theta synchronizes the activity of medial prefrontal neurons during learning. Learn Mem 15:524-531.
33. Penfield W, Welch K (1951) The supplementary motor area of the cerebral cortex; a clinical and experimental study. AMA Arch Neurol Psychiatry 66:289-317.
34. 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.
35. Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846-850.
36. Shidara M, Mizuhiki T, Richmond BJ (2005) Neuronal firing in anterior cingulate neurons changes modes across trials in single states of multitrial reward schedules. Exp Brain Res 163:242-245.
37. Showers MJ (1959) The cingulate gyrus: additional motor area and cortical autonomic regulator. J Comp Neurol 112:231-301.
38. Sinnamon HM, Galer BS (1984) Head movements elicited by electrical stimulation of the anteromedial cortex of the rat. Physiol Behav 33:185-190.
39. Steenland HW, Zhuo M (2009) Neck electromyography is an effective measure of fear behavior. J Neurosci Methods 177:355-360.
40. Steenland HW, Wu V, Fukushima H, Kida S, Zhuo M (2010) CaMKIV forebrain overexpression boosts cortical 4-7Hz oscillations during learning and 1-4 Hz delta oscillations during sleep. Mol Brain 3:16.
41. Takenouchi K, Nishijo H, Uwano T, Tamura R, Takigawa M, Ono T (1999) Emotional and behavioral correlates of the anterior cingulate cortex during associative learning in rats. Neuroscience 93:1271-1287.
42. Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M (2005) Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 1:6.
43. Tsai ML, Kuo CC, Sun WZ, Yen CT (2004) Differential morphine effects on short-and long-latency laser-evoked cortical responses in the rat. Pain 110:665-674.
44. Tsujimoto T, Shimazu H, Isomura Y (2006) Direct recording of theta oscillations in primate prefrontal and anterior cingulate cortices. J Neurophysiol 95:2987-3000.
45. Wu LJ, Zhang XH, Fukushima H, Zhang F, Wang H, Toyoda H, Li BM, Kida S, Zhuo M (2008) Genetic enhancement of trace fear memory and cingulate potentiation in mice overexpressing Ca2+/calmodulin-dependent protein kinase IV. Eur J Neurosci 27:1923-1932.
46. Zhao MG, Toyoda H, Ko SW, Ding HK, Wu LJ, Zhuo M (2005) Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J Neurosci 25:7385-7392.
47. Zhao MG, Ko SW, Wu LJ, Toyoda H, Xu H, Quan J, Li J, Jia Y, Ren M, Xu ZC, Zhuo M (2006) Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J Neurosci 26:8923-8930.