Learning-related plasticity of temporal coding in simultaneously recorded amygdala-cortical ensembles

Journal of Neuroscience

Volumn 28, Issue 11, 2008, Pages 2864-2873

  Grossman, Stephen E ^a   Fontanini, Alfredo ^a   Wieskopf, Jeffrey S ^a   Katz, Donald B ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

Basolateral amygdala; Conditioned taste aversion; Electrophysiology; Gustatory cortex; Single unit; Taste

Indexed keywords

SACCHARIN;

AMYGDALOID NUCLEUS; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; LEARNING; MALE; MEMORY; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; RAT; SOMATOSENSORY SYSTEM; TASTE; TASTE AVERSION;

AMYGDALA; ANIMALS; CEREBRAL CORTEX; FEMALE; LEARNING; MALE; NEURAL PATHWAYS; NEURONAL PLASTICITY; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 40849094658     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4063-07.2008     Document Type: Article

References (53)

1. Armony JL, Quirk GJ, LeDoux JE (1998) Differential effects of amygdala lesions on early and late plastic components of auditory cortex spike trains during fear conditioning. J Neurosci 18:2592-2601.
2. Bauer EP, Paz R, Pare D (2007) Gamma oscillations coordinate amygdalorhinal interactions during learning. J Neurosci 27:9369-9379.
3. Berman DE, Dudai Y (2001) Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291:2417-2419.
4. Bermudez-Rattoni F, Grijalva CV, Kiefer SW, Garcia J (1986) Flavor-illness aversions: the role of the amygdala in the acquisition of taste-potentiated odor aversions. Physiol Behav 38:503-508.
5. Berridge KC (2000) Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci Biobehav Rev 24:173-198.
6. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369.
7. Breslin PA, Spector AC, Grill HJ (1992) A quantitative comparison of taste reactivity behaviors to sucrose before and after lithium chloride pairings: a unidimensional account of palatability. Behav Neurosci 106:820-836.
8. Bures J, Bermúdez-Rattoni F, Yamamoto T (1998) Conditioned taste aversion: memory of a special kind. Oxford: Oxford UP.
9. Buresova O, Aleksanyan ZA, Bures J (1979) Electrophysiological analysis of retrieval of conditioned taste aversion in rats. Unit activity changes in critical brain regions. Physiologia Bohemoslovaca 28:525-536.
10. Di Lorenzo PM, Schwartzbaum JS (1982) Coding of gustatory information in the pontine parabrachial nuclei of the rabbit: temporal patterns of neural response. Brain Res 251:245-257.
11. Escobar ML, Bermudez-Rattoni F (2000) Long-term potentiation in the insular cortex enhances conditioned taste aversion retention. Brain Res 852:208-212.
12. Escobar ML, Chao V, Bermudez-Rattoni F (1998a) In vivo long-term potentiation in the insular cortex: NMDA receptor dependence. Brain Res 779:314-319.
13. Escobar ML, Alcocer I, Chao V (1998b) The NMDA receptor antagonist CPP impairs conditioned taste aversion and insular cortex long-term potentiation in vivo. Brain Res 812:246-251.
14. Escobar ML, Alcocer I, Bermudez-Rattoni F (2002) In vivo effects of intracortical administration of NMDA and metabotropic glutamate receptors antagonists on neocortical long-term potentiation and conditioned taste aversion. Behav Brain Res 129:101-106.
15. Ferreira G, Miranda MI, De la Cruz V, Rodriguez-Ortiz CJ, Bermudez-Rattoni F (2005) Basolateral amygdala glutamatergic activation enhances taste aversion through NMDA receptor activation in the insular cortex. Eur J Neurosci 22:2596-2604.
16. Fontanini A, Katz DB (2006) State-dependent modulation of time-varying gustatory responses. J Neurophysiol 96:3183-3193.
17. Frank ME, Formaker BK, Hettinger TP (2003) Taste responses to mixtures: analytic processing of quality. Behav Neurosci 117:228-235.
18. 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.
19. Grill HJ, Norgren R (1978) The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143:263-279.
20. Gutierrez R, Carmena JM, Nicolelis MA, Simon SA (2006) Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J Neurophysiol 95:119-133.
21. Halpern BP, Tapper DN (1971) Taste stimuli: quality coding time. Science 171:1256-1258.
22. Jones MW, French PJ, Bliss TV, Rosenblum K (1999) Molecular mechanisms of long-term potentiation in the insular cortex in vivo. J Neurosci 19:RC36(1-8).
23. Katz DB, Steinmetz JE (1997) Single-unit evidence for eye-blink conditioning in cerebellar cortex is altered, but not eliminated, by interpositus nucleus lesions. Learn Mem 4:88-104.
24. Katz DB, Simon SA, Nicolelis MA (2001a) Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci 21:4478-4489.
25. Katz DB, Simon SA, Nicolelis MAL (2001b) Electrophysiological studies of gustation in awake rats. In: Methods and frontiers in the chemical senses (Simon SA, Nicolelis MAL, eds), pp 339-357. Boca Raton, FL: CRC.
26. Katz DB, Simon SA, Nicolelis MA (2002) Taste-specific neuronal ensembles in the gustatory cortex of awake rats. J Neurosci 22:1850-1857.
27. Miranda MI, Ferreira G, Ramirez-Lugo L, Bermudez-Rattoni F (2002) Glutamatergic activity in the amygdala signals visceral input during taste memory formation. Proc Natl Acad Sci USA 99:11417-11422.
28. Nachman M, Ashe JH (1973) Learned taste aversions in rats as a function of dosage, concentration, and route of administration of LiCl. Physiol Behav 10:73-78.
29. Nachman M, Ashe JH (1974) Effects of basolateral amygdala lesions on neophobia, learned taste aversions, and sodium appetite in rats. J Comp Physiol Psychol 87:622-643.
30. Nicolelis MAL, Ghazanfar AA, Faggin BM, Votaw S, Oliveira LMO (1997) Reconstructing the engram: simultaneous, multisite, many single neuron recordings. Neuron 18:529-537.
31. Nishijo H, Uwano T, Tamura R, Ono T (1998) Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. J Neurophysiol 79:21-36.
32. Nitschke JB, Sarinopoulos I, Mackiewicz KL, Schaefer HS, Davidson RJ (2006) Functional neuroanatomy of aversion and its anticipation. NeuroImage 29:106-116.
33. Norgren R, Leonard CM (1973) Ascending central gustatory pathways. J Comp Neurol 150:217-237.
34. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7:419-440.
35. Quirk GJ, Repa C, LeDoux JE (1995) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15:1029-1039.
36. 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.
37. Reilly S, Bornovalova MA (2005) Conditioned taste aversion and amygdala lesions in the rat: a critical review. Neurosci Biobehav Rev 29:1067-1088.
38. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4:724-731.
39. Rollins BL, Stines SG, McGuire HB, King BM (2001) Effects of amygdala lesions on body weight, conditioned taste aversion, and neophobia. Physiol Behav 72:735-742.
40. Schafe GE, Bernstein IL (1998) Forebrain contribution to the induction of a brainstem correlate of conditioned taste aversion. II. Insular (gustatory) cortex. Brain Res 800:40-47.
41. Schafe GE, Thiele TE, Bernstein IL (1998) Conditioning method dramatically alters the role of amygdala in taste aversion learning. Learn Mem 5:481-492.
42. Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T (2003) Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39:701-711.
43. Spector AC, Breslin P, Grill HJ (1988) Taste reactivity as a dependent measure of the rapid formation of conditioned taste aversion: a tool for the neural analysis of taste-visceral associations. Behav Neurosci 102:942-952.
44. Stapleton JR, Lavine ML, Wolpert RL, Nicolelis MA, Simon SA (2006) Rapid taste responses in the gustatory cortex during licking. J Neurosci 26:4126-4138.
45. Stone ME, Grimes BS, Katz DB (2005) Hippocampal inactivation enhances taste learning. Learn Mem 12:579-586.
46. Stopfer M, Jayaraman V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39:991-1004.
47. Travers JB, Norgren R (1986) Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat. Behav Neurosci 100:544-555.
48. Wang Y-Y, Fontanini A, Katz DB (2006) Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats. Learn Mem 13:794-800.
49. Yamamoto T, Azuma S, Kawamura Y (1984) Functional relations between the cortical gustatory area and the amygdala: electrophysiological and behavioral studies in rats. Exp Brain Res 56:23-31.
50. Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1988) Sensory inputs from the oral region to the cerebral cortex in behaving rats: an analysis of unit responses in cortical somatosensory and taste areas during ingestive behavior. J Neurophysiol 60:1303-1321.
51. Yasoshima Y, Yamamoto T (1998) Short-term and long-term excitability changes of the insular cortical neurons after the acquisition of taste aversion learning in behaving rats. Neuroscience 84:1-5.
52. Yasoshima Y, Shimura T, Yamamoto T (1995a) Single unit responses of the amygdala after conditioned taste aversion in conscious rats. NeuroReport 6:2424-2428.
53. Yasoshima Y, Shimura T, Yamamoto T (1995b) Changes of taste responses in the insular cortex in freely behaving rats after acquisition of conditioned taste aversion learning. Jpn J Physiol 45:S188.