Amygdala stimulation evokes time-varying synaptic responses in the gustatory cortex of anesthetized rats

Frontiers in Integrative Neuroscience

Volumn 5, Issue , 2011, Pages

  Stone, Martha E ^a   Maffei, Arianna ^a   Fontanini, Alfredo ^a  

^a Stony Brook University   (United States)

Author keywords

Amygdala; Hedonics; In vivo intracellular; Taste; Top down

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED CORTICAL RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC SYSTEM; GLUTAMATERGIC POTENTIAL; GUSTATORY CORTEX; HYPERPOLARIZATION; IN VIVO STUDY; LATENT PERIOD; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; PREDICTION; RAT; SENSORY NERVE CELL; SENSORY NERVE CONDUCTION; TIME VARYING EVOKED RESPONSE;

EID: 82255191392     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2011.00003     Document Type: Article

References (69)

1. Aggleton, J. P., Burton, M. J., and Passingham, R. E. (1980). Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res. 190, 347-368.
2. Allen, G. V., Saper, C. B., Hurley, K. M., and Cechetto, D. F. (1991). Organization of visceral and limbic connections in the insular cortex of the rat. J. Comp. Neurol. 311, 1-16.
3. Aroniadou-Anderjaska, V., Fritsch, B., Qashu, F., and Braga, M. F. (2008). Pathology and pathophysiology of the amygdala in epileptogenesis and epilepsy. Epilepsy Res. 78, 102-116.
4. Avoli, M., D'Antuono, M., Louvel, J., Kohling, R., Biagini, G., Pumain, R., D'Arcangelo, G., and Tancredi, V. (2002). Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog. Neurobiol. 68, 167-207.
5. Balleine, B. W., and Killcross, S. (2006). Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci. 29, 272-279.
6. Beierlein, M., Gibson, J. R., and Connors, B. W. (2003). Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987-3000.
7. Bermudez-Rattoni, F., Grijalva, C. V., Kiefer, S. W., and Garcia, J. (1986). Flavor-illness aversions: the role of the amygdala in the acquisition of taste-potentiated odor aversions. Physiol. Behav. 38, 503-508.
8. Blood, A. J., and Zatorre, R. J. (2001). Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc. Natl. Acad. Sci. U.S.A. 98, 11818-11823.
9. Bordi, F., and LeDoux, J. E. (1994). Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdala stimulation. Exp. Brain Res. 98, 275-286.
10. Bornhovd, K., Quante, M., Glauche, V., Bromm, B., Weiller, C., and Buchel, C. (2002). Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. Brain 125(Pt 6), 1326-1336.
11. Breiter, H. C., Gollub, R. L., Weisskoff, R. M., Kennedy, D. N., Makris, N., Berke, J. D., Goodman, J. M., Kantor, H. L., Gastfriend, D. R., Riorden, J. P., Mathew, R. T., Rosen, B. R., and Hyman, S. E. (1997). Acute effects of cocaine on human brain activity and emotion. Neuron 19, 591-611.
12. Breslin, P. A., Spector, A. C., and Grill, H. J. (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.
13. Chavez, C. M., McGaugh, J. L., and Weinberger, N. M. (2009). The basolateral amygdala modulates specific sensory memory representations in the cerebral cortex. Neurobiol. Learn. Mem. 91, 382-392.
14. Clark, E. W., and Bernstein, I. L. (2009). Boosting cholinergic activity in gustatory cortex enhances the salience of a familiar conditioned stimulus in taste aversion learning. Behav. Neurosci. 123, 764-771.
15. Cruikshank, S. J., Lewis, T. J., and Connors, B. W. (2007). Synaptic basis for intense thalamocortical activation of feed forward inhibitory cells in neocortex. Nat. Neurosci. 10, 462-468.
16. Cruikshank, S. J., Urabe, H., Nurmikko, A. V., and Connors, B. W. (2010). Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65, 230-245.
17. Doucette, W., and Restrepo, D. (2008). Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 6, e258. doi: 10.1371/journal.pbio.0060258
18. Dunckley, P., Wise, R. G., Aziz, Q., Painter, D., Brooks, J., Tracey, I., and Chang, L. (2005). Cortical processing of visceral and somatic stimulation: differentiating pain intensity from unpleasantness. Neuroscience 133, 533-542.
19. Escobar, M. L., Alcocer, I., and 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.
20. Escobar, M. L., and Bermudez-Rattoni, F. (2000). Long-term potentiation in the insular cortex enhances conditioned taste aversion retention. Brain Res. 852, 208-212.
21. Ferreira, G., Miranda, M. I., De la Cruz, V., Rodríguez-Ortiz, C. J., and Bermúdez-Rattoni, F. (2005). Basolateral amygdala glutamatergic activation enhances taste aversion through NMDA receptor activation in the insular cortex. Eur. J. Neurosci. 22, 2596-2604.
22. Fontanini, A., Grossman, S. E., Figueroa, J. A., and Katz, D. B. (2009). Distinct subtypes of basolateral amygdale taste neurons reflect palatability and reward. J. Neurosci. 29, 2486-2495.
23. Fontanini, A., and Katz, D. B. (2005). 7 to 12 Hz activity in rat gustatory cortex reflects disengagement from a fluid self-administration task. J. Neurophysiol. 93, 2832-2840.
24. Fontanini, A., and Katz, D. B. (2006). State-dependent modulation of time-varying gustatory responses. J. Neurophysiol. 96, 3183-3193.
25. Fontanini, A., and Katz, D. B. (2008). Behavioral states, network states, and sensory response variability. J. Neurophysiol. 100, 1160-1168.
26. Fontanini, A., Spano, P., and Bower, J. M. (2003). Ketamine-xylazine-induced slow (<1.5 Hz) oscillations in the rat piriform (olfactory) cortex are functionally correlated with respiration. J. Neurosci. 23, 7993-8001.
27. Fujita, S., Adachi, K., Koshikawa, N., and Kobayashi, M. (2010). Spatiotemporal dynamics of excitation in rat insular cortex: intrinsic corticocortical circuit regulates caudal-rostro excitatory propagation from the insular to frontal cortex. Neuroscience 165, 278-292.
28. Gallo, M., Roldan, G., and 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.
29. Grossman, S. E., Fontanini, A., Wieskopf, J. S., and Katz, D. B. (2008). Learning-related plasticity of temporal coding in simultaneously recorded amygdala-cortical ensembles. J. Neurosci. 28, 2864-2873.
30. Haberly, L. B., and Bower, J. M. (1984). Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. J. Neurophysiol. 51, 90-112.
31. Hanamori, T. (2009). Effects of electrical and chemical stimulation of the amygdala on the spontaneous discharge in the insular cortex in rats. Brain Res. 1276, 91-102.
32. Hasenstaub, A., Sachdev, R. N., and McCormick, D. A. (2007). State changes rapidly modulate cortical neuronal responsiveness. J. Neurosci. 27, 9607-9622.
33. Holland, P. C., and Gallagher, M. (2004). Amygdala-frontal interactions and reward expectancy. Curr. Opin. Neurobiol. 14, 148-155.
34. Inaba, Y., De Guzman, P., and Avoli, M. (2006). NMDA receptor-mediated transmission contributes to network 'hyperexcitability' in the rat insular cortex. Eur. J. Neurosci. 23, 1071-1076.
35. Jones, L. M., Fontanini, A., and Katz, D. B. (2006). Gustatory processing: a dynamic systems approach. Curr. Opin. Neurobiol. 16, 420-428.
36. Jones, L. M., Fontanini, A., Sadacca, B. F., Miller, P., and Katz, D. B. (2007). Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles. Proc. Natl. Acad. Sci. U.S.A. 104, 18772-18777.
37. Jones, M. W., French, P. J., Bliss, T. V. P., and Rosenblum, K. (1999). Molecular mechanisms of long-term potentiation in the insular cortex in vivo. J. Neurosci. 19, 36RC1-36RC8.
38. Kang, Y., and Lundy, R. F. (2010). Amygdalofugal influence on processing of taste information in the nucleus of the solitary tract of the rat. J. Neurophysiol. 104, 726-741.
39. Katz, D. B., Nicolelis, M. A., and Simon, S. A. (2002). Gustatory processing is dynamic and distributed. Curr. Opin. Neurobiol. 12, 448-454.
40. Katz, D. B., Simon, S. A., and Nicolelis, M. A. (2001). Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J. Neurosci. 21, 4478-4489.
41. Li, C. S., Cho, Y. K., and Smith, D. V. (2002). Taste responses of neurons in the hamster solitary nucleus are modulated by the central nucleus of the amygdala. J. Neurophysiol. 88, 2979-2992.
42. Li, C. S., Cho, Y. K., and Smith, D. V. (2005). Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala. J. Neurophysiol. 93, 1183-1196.
43. Maffei, A., Nataraj, K., Nelson, S. B., and Turrigiano, G. G. (2006). Potentiation of cortical inhibition by visual deprivation. Nature 443, 81-84.
44. Miller, P., and Katz, D. B. (2010). Stochastic transitions between neural states in taste processing and decision-making. J. Neurosci. 30, 2559-2570.
45. Moore, C. I., and Nelson, S. B. (1998). Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80, 2882-2892.
46. Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., and Dolan, R. J. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812-815.
47. Nishijo, H., Ono, T., and Nishino, H. (1988). Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance. J. Neurosci. 8, 3570-3583.
48. Nishijo, H., Uwano, T., Tamura, R., and 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.
49. Ogawa, H., Hasegawa, K., Otawa, S., and Ikeda, I. (1998). GABAergic inhibition and modifications of taste responses in the cortical taste area in rats. Neurosci. Res. 32, 85-95.
50. Ohara, P. T., Granato, A., Moallem, T. M., Wang, B. R., Tillet, Y., and Jasmin, L. (2003). Dopaminergic input to GABAergic neurons in the rostral agranular insular cortex of the rat. J. Neurocytol. 32, 131-141.
51. Ortigue, S., Grafton, S. T., and Bianchi-Demicheli, F. (2007). Correlation between insula activation and self-reported quality of orgasm in women. Neuroimage 37, 551-560.
52. Pantoja, J., Ribeiro, S., Wiest, M., Soares, E., Gervasoni, D., Lemos, N. A., and Nicolelis, M. A. (2007). Neuronal activity in the primary somatosensory thalamocortical loop is modulated by reward contingency during tactile discrimination. J. Neurosci. 27, 10608-10620.
53. Paton, J. J., Belova, M. A., Morrison, S. E., and Salzman, C. D. (2006). The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865-870.
54. Quirk, G. J., Armony, J. L., and LeDoux, J. E. (1997). Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19, 613-624.
55. Reilly, S., and Bornovalova, M. A. (2005). Conditioned taste aversion and amygdala lesions in the rat: a critical review. Neurosci. Biobehav. Rev. 29, 1067-1088.
56. Remedios, R., Logothetis, N. K., and Kayser, C. (2009). An auditory region in the primate insular cortex responding preferentially to vocal communication sounds. J. Neurosci. 29, 1034-1045.
57. Roesch, M. R., Calu, D. J., Esber, G. R., and Schoenbaum, G. (2010). All that glitters... dissociating attention and outcome expectancy from prediction errors signals. J. Neurophysiol. 104, 587-595.
58. Saper, C. B. (1982). Convergence of autonomic and limbic connections in the insular cortex of the rat. J. Comp. Neurol. 210, 163-173.
59. Schafe, G. E., Thiele, T. E., and Bernstein, I. L. (1998). Conditioning method dramatically alters the role of amygdala in taste aversion learning. Learn. Mem. 5, 481-492.
60. Schoenbaum, G., Setlow, B., Nugent, S. L., Saddoris, M. P., and Gallagher, M. (2003). Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn. Mem. 10, 129-140.
61. Shuler, M. G., and Bear, M. F. (2006). Reward timing in the primary visual cortex. Science 311, 1606-1609.
62. Small, D. M., Zatorre, R. J., Dagher, A., Evans, A. C., and Jones-Gotman, M. (2001). Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 124(Pt 9), 1720-1733.
63. Travers, J. B., and Norgren, R. (1986). Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat. Behav. Neurosci. 100, 544-555.
64. Wang, Y., Fontanini, A., and Katz, D. B. (2006). Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats. Learn. Mem. 13, 794-800.
65. Yamamoto, K., Koyanagi, Y., Koshikawa, N., and Kobayashi, M. (2010). Postsynaptic cell type-dependent cholinergic regulation of GABAergic synaptic transmission in rat insular cortex. J. Neurophysiol. 104, 1933-1945.
66. Yamamoto, T., Azuma, S., and Kawamura, Y. (1984a). Functional relations between the cortical gustatory area and the amygdala: electrophysiological and behavioral studies in rats. Exp. Brain Res. 56, 23-31.
67. Yamamoto, T., Yuyama, N., Kato, T., and Kawamura, Y. (1984b). Gustatory responses of cortical neurons in rats. I. Response characteristics. J. Neurophysiol. 51, 616-635.
68. Yamamoto, T., Yuyama, N., and Kawamura, Y. (1981). Cortical neurons responding to tactile, thermal and taste stimulations of the rat's tongue. Brain Res. 221, 202-206.
69. Yokota, T., Eguchi, K., and Satoh, T. (2007). Differential taste coding of salt and acid by correlative activities between taste-sensitive neuron types in rat gustatory cortex. Neuroscience 144, 314-324.