The indirect amygdala-dorsal striatum pathway mediates conditioned freezing: Insights on emotional memory networks

Neuroscience

Volumn 153, Issue 1, 2008, Pages 84-94

  Ferreira, T L ^a   Shammah Lagnado, S J ^b   Bueno, O F A ^a   Moreira, K M ^a   Fornari, R V ^a   Oliveira, M G M ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

asymmetrical lesions; caudate; central amygdaloid nucleus; contextual fear conditioning; learning; tone fear conditioning

Indexed keywords

MUSCIMOL;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FREEZING; HISTOPATHOLOGY; LEARNING; MALE; MEMORY; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA; SYNAPSE;

AMYGDALA; ANIMALS; CONDITIONING (PSYCHOLOGY); CORPUS STRIATUM; DENERVATION; ELECTRIC STIMULATION; EMOTIONS; FEAR; FREEZING REACTION, CATALEPTIC; FUNCTIONAL LATERALITY; GABA AGONISTS; MALE; NERVE NET; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; RATS; RATS, WISTAR;

EID: 41949101582     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.02.013     Document Type: Article

References (75)

1. Anglada-Figueroa D., and Quirk G.J. Lesions of the basal amygdala block expression of conditioned fear but not extinction. J Neurosci 25 (2005) 9680-9685
2. Aosaki T., Graybiel A.M., and Kimura M. Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265 (1994) 412-415
3. Aosaki T., Tsubokawa H., Ishida A., Watanabe K., Graybiel A.M., and Kimura M. Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14 (1994) 3969-3984
4. Barnes T.D., Kubota Y., Hu D., Jin D.Z., and Graybiel A.M. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437 (2005) 1158-1161
5. Beckstead R.M., Domesick V.B., and Nauta W.J. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175 (1979) 191-217
6. Beitz A.J. The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7 (1982) 133-159
7. Blair H.T., Schafe G.E., Bauer E.P., Rodrigues S.M., and LeDoux J.E. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8 (2001) 229-242
8. Blanchard D.C., and Blanchard R.J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol 81 (1972) 281-290
9. Blazquez P.M., Fujii N., Kojima J., and Graybiel A.M. A network representation of response probability in the striatum. Neuron 33 (2002) 973-982
10. Bueno O.F.A., Oliveira M.G.M., Pomarico A.C., and Gugliano E.B. A dissociation between the proactive ECS effects on inhibitory avoidance learning and on classical fear conditioning. Behav Neural Biol 59 (1993) 180-185
11. Campeau S., and Davis M. Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15 (1995) 2312-2327
12. Carrive P., Lee J., and Su A. Lidocaine blockade of amygdala output in fear-conditioned rats reduces Fos expression in the ventrolateral periaqueductal gray. Neuroscience 95 (2000) 1071-1080
13. Carrive P., Leung P., Harris J., and Paxinos G. Conditioned fear to context is associated with increased Fos expression in the caudal ventrolateral region of the midbrain periaqueductal gray. Neuroscience 78 (1997) 165-177
14. Cebrian C., Parent A., and Prensa L. Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat. J Comp Neurol 492 (2005) 349-369
15. Cromwell H.C., and Berridge K.C. Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax. J Neurosci 16 (1996) 3444-3458
16. Cruz-Morales S.E., Duran-Arevalo M., Diaz Del Guante M.A., Quirarte G., and Prado-Alcala R.A. A threshold for the protective effect of over-reinforced passive avoidance against scopolamine-induced amnesia. Behav Neural Biol 57 (1992) 256-259
17. Deutch A.Y., Goldstein M., Baldino Jr. F., and Roth R.H. Telencephalic projections of the A8 dopamine cell group. Ann N Y Acad Sci 537 (1988) 27-50
18. Fanselow M.S., and Bolles R.C. Naloxone and shock-elicited freezing in the rat. J Comp Physiol Psychol 93 (1979) 736-744
19. Fendt M., and Fanselow M.S. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 23 (1999) 743-760
20. Ferreira T.L., Moreira K.M., Ikeda D.C., Bueno O.F.A., and Oliveira M.G.M. Effects of dorsal striatum lesions in tone fear conditioning and contextual fear conditioning. Brain Res 987 (2003) 17-24
21. Fornari R.V., Moreira K.M., and Oliveira M.G.M. Effects of the selective M1 muscarinic receptor antagonist dicyclomine on emotional memory. Learn Mem 7 (2000) 287-292
22. Fudge J.L., and Haber S.N. The central nucleus of the amygdala projection to dopamine subpopulations in primates. Neuroscience 97 (2000) 479-494
23. Gallagher M., Graham P.W., and Holland P.C. The amygdala central nucleus and appetitive pavlovian conditioning: lesions impair one class of conditioned behavior. J Neurosci 10 (1990) 1906-1911
24. Gastard M., Jensen S.L., Martin III J.R., Williams E.A., and Zahm D.S. The caudal sublenticular region/anterior amygdaloid area is the only part of the rat forebrain and mesopontine tegmentum occupied by magnocellular cholinergic neurons that receives outputs from the central division of extended amygdala. Brain Res 957 (2002) 207-222
25. Gerfen C.R., Herkenham M., and Thibault J. The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7 (1987) 3915-3934
26. Goldstein L.E., Rasmusson A.M., Bunney B.S., and Roth R.H. Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16 (1996) 4787-4798
27. Gonzales C., and Chesselet M.F. Amygdalonigral pathway: an anterograde study in the rat with Phaseolus vulgaris leucoagglutinin (PHA-L). J Comp Neurol 297 (1990) 182-200
28. Goosens K.A., and Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn Mem 8 (2001) 148-155
29. Han J.S., McMahan R.W., Holland P.C., and Gallagher M. The role of an amygdalo-nigrostriatal pathway in associative learning. J Neurosci 17 (1997) 3913-3919
30. Heimer L., Zahm D.S., and Alheid G.F. Basal ganglia. In: Paxinos G. (Ed). The rat nervous system. 2nd ed. (1995), Academic Press, San Diego 579-648
31. Hitchcock J.M., and Davis M. Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm. Behav Neurosci 105 (1991) 826-842
32. Kapp B.S., Frysinger R.C., Gallagher M., and Haselton J.R. Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol Behav 23 (1979) 1109-1117
33. Kim J.J., and Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 256 (1992) 675-677
34. Kim J.J., Rison R.A., and Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 107 (1993) 1093-1098
35. Kirouac G.J., Li S., and Mabrouk G. GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus. J Comp Neurol 469 (2004) 170-184
36. LeDoux J.E. Emotional memory systems in the brain. Behav Brain Res 58 (1993) 69-79
37. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 23 (2000) 155-184
38. LeDoux J.E., Iwata J., Cicchetti P., and Reis D.J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8 (1988) 2517-2529
39. LeDoux J.E., Sakaguchi A., Iwata J., and Reis D.J. Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli. Neuroscience 17 (1986) 615-627
40. Lee H.J., Groshek F., Petrovich G.D., Cantalini J.P., Gallagher M., and Holland P.C. Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J Neurosci 25 (2005) 3881-3888
41. Ljungberg T., Apicella P., and Schultz W. Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67 (1992) 145-163
42. Malkani S., and Rosen J.B. Specific induction of early growth response gene 1 in the lateral nucleus of the amygdala following contextual fear conditioning in rats. Neuroscience 97 (2000) 693-702
43. Maren S. Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. J Neurosci 19 (1999) 8696-8703
44. Maren S. Neurobiology of pavlovian fear conditioning. Annu Rev Neurosci 24 (2001) 897-931
45. Maren S., Aharonovm G., and Fanselow M.S. Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: absence of a temporal gradient. Behav Neurosci 110 (1996) 718-726
46. Mirenowicz J., and Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379 (1996) 449-451
47. Nader K., Majidishad P., Amorapanth P., and LeDoux J.E. Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learn Mem 8 (2001) 156-163
48. Packard M.G., Hirsh R., and White N.M. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9 (1989) 1465-1472
49. Packard M.G., and McGaugh J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav Neurosci 106 (1992) 439-446
50. Paré D., Quirk G.J., and LeDoux J.E. New vistas on amygdala networks in conditioned fear. J Neurophysiol 92 (2004) 1-9
51. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1997), Academic Press, San Diego
52. Peyron C., Petit J.M., Rampon C., Jouvet M., and Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 82 (1998) 443-468
53. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106 (1992) 274-285
54. Pitkänen A. Connectivity of the rat amygdaloid complex. In: Aggleton J.P. (Ed). The amygdala: a functional analysis. 2nd ed. (2000), Oxford University Press, Oxford 31-115
55. Powell D.A., Mankowski D., and Buchanan S. Concomitant heart rate and corneoretinal potential conditioning in the rabbit (Oryctolagus cuniculus): effects of caudate lesions. Physiol Behav 20 (1978) 143-150
56. Ravel S., Legallet E., and Apicella P. Tonically active neurons in the monkey striatum do not preferentially respond to appetitive stimuli. Exp Brain Res 28 (1999) 531-534
57. Ravel S., Legallet E., and Apicella P. Responses of tonically active neurons in the monkey striatum discriminate between motivationally opposing stimuli. J Neurosci 23 (2003) 8489-8497
58. Rizvi T.A., Ennis M., Behbehani M.M., and Shipley M.T. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303 (1991) 121-131
59. Rodriguez M., Abdala P., Barroso-Chinea P., and Gonzalez-Hernandez T. The deep mesencephalic nucleus as an output center of basal ganglia: morphological and electrophysiological similarities with the substantia nigra. J Comp Neurol 438 (2001) 12-31
60. Rye D.B., Saper C.B., Lee H.J., and Wainer B.H. Pedunculopontine tegmental nucleus of the rat: Cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259 (1987) 483-528
61. Sananes C.B., and Campbell B.A. Role of the central nucleus of the amygdala in olfactory heart rate conditioning. Behav Neurosci 103 (1989) 519-525
62. Schultz W., Tremblay L., and Hollerman J.R. Changes in behavior-related neuronal activity in the striatum during learning. Trends Neurosc 26 (2003) 321-328
63. Shammah-Lagnado S.J., Alheid G., and Heimer L. Striatal and central extended amygdala parts of the interstitial nucleus of the posterior limb of the anterior commissure: evidence from tract-tracing techniques in the rat. J Comp Neurol 439 (2001) 104-126
64. Solana-Figueroa R., Salado-Castillo R., Quirarte G.L., Galindo L.E., and Prado-Alcala R.A. Enhanced inhibitory avoidance training protects against the amnesic effect of p-chloroamphetamine. Life Sci 71 (2002) 391-399
65. Spann B.M., and Grofová I. Nigropedunculopontine projection in the rat: an anterograde tracing study with Phaseolus vulgaris-leucoagglutinin (PHA-L). J Comp Neurol 311 (1991) 375-388
66. Steinbusch H.W. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6 (1981) 557-618
67. Sullivan G.M., Apergis J., Bush D.E., Johnson L.R., Hou M., and Ledoux J.E. Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128 (2004) 7-14
68. Ungless M.A., Magill P.J., and Bolam J.P. Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303 (2004) 2040-2042
69. Vertes R.P. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313 (1991) 643-668
70. Vianna D.M., Graeff F.G., Landeira-Fernandez J., and Brandão M.L. Lesion of the ventral periaqueductal gray reduces conditioned fear, but does not change freezing induced by stimulation of the dorsal periaqueductal gray. Learn Mem 8 (2001) 164-169
71. White N.M., and Salinas J.A. Mnemonic functions of dorsal striatum and hippocampus in aversive conditioning. Behav Brain Res 142 (2003) 99-107
72. Wilensky A.E., Schafe G.E., Kristensen M.P., and LeDoux J.E. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of pavlovian fear conditioning. J Neurosci 26 (2006) 12387-12396
73. Yamada H., Matsumoto N., and Kimura M. Tonically active neurons in the primate caudate nucleus and putamen differentially encode instructed motivational outcomes of action. J Neurosci 24 (2004) 3500-3510
74. Zahm D.S., Jensen S.L., Williams E.S., and Martin III J.R. Direct comparison of projections from the central amygdaloid region and nucleus accumbens shell. Eur J Neurosci 11 (1999) 1119-1126
75. Zimmerman J.M., Rabinak C.A., McLachlan I.G., and Maren S. The central nucleus of the amygdala is essential for acquiring and expressing conditional fear after overtraining. Learn Mem 14 (2007) 634-644