Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning

European Journal of Neuroscience

Volumn 27, Issue 11, 2008, Pages 3043-3049

  Lee, H J ^a   Youn, J M ^a   Gallagher, M ^a   Holland, P C ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Associative learning; Midbrain dopamine; Prediction error; Rat

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CANNULA; DOPAMINERGIC NERVE CELL; HEMISPHERIC DOMINANCE; LEARNING THEORY; MALE; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA;

AMYGDALA; ANIMALS; ASSOCIATION LEARNING; ATTENTION; BEHAVIOR, ANIMAL; COGNITION; CONDITIONING, CLASSICAL; CUES; DENERVATION; FUNCTIONAL LATERALITY; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; RATS; RATS, LONG-EVANS; REACTION TIME; REINFORCEMENT (PSYCHOLOGY); SUBSTANTIA NIGRA; TIME FACTORS; TIME PERCEPTION;

EID: 45349085647     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06272.x     Document Type: Article

References (42)

1. Baxter, M. G., Holland, P.C. Gallagher, M. (1997) Disruption of decrements in conditioned stimulus processing by selective removal of hippocampal cholinergic input. J. Neurosci., 17, 5230 5236.
2. Briand, L.A., Gritton, H., Howe, W.M., Young, D.A. Sarter, M. (2007) Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog. Neurobiol., 83, 69 91.
3. Bucci, D.J. Macleod, J.E. (2007) Changes in neural activity associated with a surprising change in the predictive validity of a conditioned stimulus. Eur. J. Neurosci., 26, 2669 2676.
4. Bucci, D.J., Holland, P.C. Gallagher, M. (1998) Removal of cholinergic input to rat posterior parietal cortex disrupts incremental processing of conditioned stimuli. J. Neurosci., 18, 8038 8046.
5. Chen, B.T. Rice, M.E. (2002) Synaptic regulation of somatodendritic dopamine release by glutamate and GABA differs between substantia nigra and ventral tagmental area. J. Neurochem., 81, 158 169.
6. Chiba, A.A., Bucci, D.J., Holland, P.C. Gallagher, M. (1995) Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J. Neurosci., 15, 7315 7322.
7. Christoffersen, C.L. Meltzer, L.T. (1995) Evidence for N-methyl-d-aspartate and AMPA subtypes of the glutamate receptor on substantia nigra dopamine neurons: possible preferential role for N-methyl-d-aspartate receptors. Neuroscience, 67, 373 381.
8. El-Amamy, H. Holland, P.C. (2006) Substantia nigra pars compacta is critical to both the acquisition and expression of learned orienting of rats. Eur. J. Neurosci., 24, 270 276.
9. Emmi, A., Rajabi, H. Stewart, J. (1997) Behavioral and neurochemical recovery from partial 6-hydroxydopamine lesions of the substantia nigra is blocked by daily treatment with D1/D5, but not D2, dopamine receptor antagonists. J. Neurosci., 17, 3840 3846.
10. Fallon, J.H. Loughlin, S.E. (1995) Substantia nigra. In Paxinos, G. (Ed. The Rat Nervous System, Academic Press, San Diego, pp. 215 237.
11. Fallon, J.H. Moore, R.Y. (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol., 180, 545 580.
12. Fudge, J.L. Haber, S.N. (2000) The central nucleus of the amygdala projection to dopamine subpopulations in primates. Neuroscience, 97, 479 494.
13. Gallagher, M., Graham, P.W. Holland, P.C. (1990) The amygdala central nucleus and appetitive pavlovian conditioning: lesions impair one class of conditioned behavior. J. Neurosci., 10, 1906 1911.
14. Gaykema, R.P. Zaborszky, L. (1996) Direct catecholaminergic-cholinergic interactions in the basal forebrain. II. Substantia nigra-ventral tegmental area projections to cholinergic neurons. J. Comp. Neurol., 374, 555 577.
15. Gonzales, C. Chesselet, M.F. (1990) Amygdalonigral pathway: an anterograde study in the rat with Phaseolus vulgaris leucoagglutinin (PHA-L). J. Comp. Neurol., 297, 182 200.
16. Grove, E.A. (1988) Neural associations of the substantia innominata in the rat: afferent connections. J. Comp. Neurol., 277, 315 346.
17. Han, J.S., McMahan, R.W., Holland, P.C. Gallagher, M. (1997) The role of an amygdalo-nigrostriatal pathway in associative learning. J. Neurosci., 17, 3913 3919.
18. Han, J.S., Holland, P.C. Gallagher, M. (1999) Disconnection of the amygdala central nucleus and substantia innominata/nucleus basalis disrupts increments in conditioned stimulus processing in rats. Behav. Neurosci., 113, 143 151.
19. Hasue, R.H. Shammah-Lagnado, S.J. (2002) Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat. J. Comp. Neurol., 454, 15 33.
20. Holland, P.C. (1977) Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J. Exp. Psychol. Anim. Behav. Process., 3, 77 104.
21. Holland, P.C. Gallagher, M. (1993) Amygdala central nucleus lesions disrupt increments, but not decrements, in conditioned stimulus processing. Behav. Neurosci., 107, 246 253.
22. Holland, P.C. Gallagher, M. (1999) Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci., 3, 65 73.
23. Holland, P.C. Gallagher, M. (2006) Different roles for amygdala central nucleus and substantia innominata in the surprise-induced enhancement of learning. J. Neurosci., 26, 3791 3797.
24. Jolkkonen, E., Miettinen, R., Pikkarainen, M. Pitkanen, A. (2002) Projections from the amygdaloid complex to the magnocellular cholinergic basal forebrain in rat. Neuroscience, 111, 133 149.
25. Lee, H.J., Groshek, F., Petrovich, G.D., Cantalini, J.P., Gallagher, M. Holland, P.C. (2005) Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J. Neurosci., 25, 3881 3888.
26. Lee, H.J., Youn, J.M., O, M.J., Gallagher, M. Holland, P.C. (2006) Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention. J. Neurosci., 26, 6077 6081.
27. Matsumoto, M. Hikosaka, O. (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature, 447, 1111 1115.
28. McDannald, M., Kerfoot, E., Gallagher, M. Holland, P.C. (2004) Amygdala central nucleus function is necessary for learning but not expression of conditioned visual orienting. Eur. J. Neurosci., 20, 240 248.
29. Mintz, M., Douglas, R.J., Tomer, R., de Villiers, A.S. Kellaway, L. (1986) Transient contralateral rotation following unilateral substantia nigra lesion reflects susceptibility of the nigrostriatal system to exhaustion by amphetamine. Life Sci., 39, 69 76.
30. Nakamura, M., Jang, I.-S., Ishibashi, H., Watanabe, S. Akaike, N. (2003) Possible roles of kainate receptors on GABAergic nerve terminals projecting to rat substantia nigra dopaminergic neurons. J. Neurophysiol., 90, 1662 1670.
31. Pearce, J.M. Hall, G. (1980) A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol. Rev., 87, 532 552.
32. Rescorla, R.A. Wagner, A.R. (1972) A theory of Pavlovian conditioning: variation in the effectiveness of reinforcement and nonreinforcement. In Black, A.H. Prokasy, W.F. (Eds Classical Conditioning II, Appleton-Century-Crofts, New York, pp. 64 99.
33. Robinson, T.E., Mocsary, Z., Camp, D.M. Whishaw, I.Q. (1994) Time course of recovery of extracellular dopamine following partial damage to the nigrostriatal dopamine system. J. Neurosci., 14, 2687 2696.
34. Sarter, M. Parikh, V. (2005) Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci., 6, 48 56.
35. Schultz, W. Dickinson, A. (2000) Neuronal coding of prediction errors. Annu. Rev. Neurosci., 23, 473 500.
36. Schultz, W., Dayan, P. Montague, P.R. (1997) A neural substrate of prediction and reward. Science, 275, 1593 1599.
37. Sun, N. Cassell, M.D. (1993) Intrinsic GABAergic neurons in the rat central extended amygdala. J. Comp. Neurol., 330, 381 404.
38. Swanson, L.W. (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull., 9, 321 353.
39. Swanson, L.W. 1992. Brain Maps: Structure of the Rat Brain. Elsevier, Amsterdam.
40. Swanson, L.W. Petrovich, G.D. (1998) What is the amygdala? Trends Neurosci., 21, 323 331.
41. Wilson, P.N., Boumphrey, P. Pearce, J.M. (1992) Restoration of the orienting response to a light by a change in its predictive accuracy. Q. J. Exp. Psychol., 44B, 17 36.
42. Yung, K.K. (1998) Localization of ionotropic and metabotropic glutamate receptors in distinct neuronal elements of the rat substantia nigra. Neurochem. Int., 33, 313 326.