Phasic activation of substantia nigra and the ventral tegmental area by chemical stimulation of the superior colliculus: An electrophysiological investigation in the rat

European Journal of Neuroscience

Volumn 17, Issue 1, 2003, Pages 28-40

  Coizet, Véronique ^a   Comoli, Eliane ^a,b   Westby, G W Max ^a   Redgrave, Peter ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Attention; Dopamine; GABA; Reward

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; BICUCULLINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGY; EVOKED RESPONSE; LATENT PERIOD; MALE; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; RAT; RECORDING; SUBSTANTIA NIGRA; SUPERIOR COLLICULUS; VENTRAL TEGMENTUM; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; BICUCULLINE; DOPAMINE; ELECTROPHYSIOLOGY; GABA ANTAGONISTS; MALE; NEURONS; RATS; SUBSTANTIA NIGRA; SUPERIOR COLLICULUS; VENTRAL TEGMENTAL AREA; VISUAL PATHWAYS;

EID: 0037236325     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02415.x     Document Type: Article

References (80)

1. Adams, J.C. (1992) Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains. J. Histochem. Cytochem., 40, 1457-1463.
2. Bar-Gad, I. & Bergman, H. (2001) Stepping out of the box: Information processing in the neural networks of the basal ganglia. Curr. Opin. Neurobiol., 11, 689-695.
3. Berridge, K.C. & Robinson, T.E. (1998) What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Res. Rev., 28, 309-369.
4. Binns, K.E. (1999) The synaptic pharmacology underlying sensory processing in the superior colliculus. Prog. Neurobiol., 59, 129-159.
5. Bolam, J.P., Francis, C.M. & Henderson, Z. (1991) Cholinergic input to dopaminergic neurons in the substantia nigra: A double immunocytochemical study. Neuroscience, 41, 483-494.
6. Brown, J., Bullock, D. & Grossberg, S. (1999) How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues. J. Neurosci., 19, 10502-10511.
7. Carter, C.J. (1982) Topographical distribution of possible glutamatergic pathways from the frontal cortex to the striatum and substantia nigra in rats. Neuropharmacology, 21, 370-383.
8. Celada, P., Paladini, C.A. & Tepper, J.M. (1999) Gabaergic control of rat substantia nigra dopaminergic neurons: Role of globus pallidus and substantia nigra pars reticulata. Neuroscience, 89, 813-825.
9. Comoli, E., Coizet, V., Canteras, N.S., Westby, G.W.M. & Redgrave, P. (2001) Direct projection from superior colliculus to dopaminergic neurones in the ventral midbrain. Soc. Neurosci. Abstr., 27, 68.11.
10. Contreras-Vidal, J.L. & Schultz, W. (1999) A predictive reinforcement model of dopamine neurons for learning approach behavior. J. Comput. Neurosci., 6, 191-214.
11. Dean, P. & Redgrave, P. (1992) Behavioural consequences of manipulating GABA neurotransmission in the superior colliculus. In Mize, R.R., Marc, R.E. & Sillito, A.M. (Eds), GABA in the Retina and Central Visual System. Prog. Brain Res. Elsevier, Amsterdam, pp. 263-281.
12. Dean, P., Redgrave, P. & Westby, G.W.M. (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci., 12, 137-147.
13. Deniau, J.M., Hammond, C., Chevalier, G. & Feger, J. (1978) Evidence for branched subthalamic nucleus projections to substantia nigra, entopedun-cular nucleus and globus pallidus. Neurosci. Lett., 9, 117-121.
14. Deniau, J.M., Kitai, S.T., Donoghue, J.P. & Grofova, I. (1982) Neuronal interactions in the substantia nigra pars reticulata through axon collateral of the projection neurons. Exp. Brain Res., 47, 105-113.
15. Doron, N.N. & LeDoux, J.E. (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J. Comp. Neurol., 412, 383-409.
16. Freeman, A.S. (1985) Firing properties of substantia nigra dopaminergic neurons in freely moving rats. Life Sci., 36, 1983-1994.
17. Gimenez-Amaya, J.M., de las Heras, S., Erro, E., Mengual, E. & Lanciego, J.L. (2000) Considerations on the thalamostriatal system with some functional implications. Histol. Histopathol., 15, 1285-1292.
18. Goldberg, M.E. & Wurtz, R.H. (1972) Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. J. Neurophysiol., 35, 560-574.
19. 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.
20. Gonzalez-Hernandez, T. & Rodriguez, M. (2000) Compartmental organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat. J. Comp. Neurol., 421, 107-135.
21. Grace, A.A. & Bunney, B.S. (1979) Paradoxical GABA excitation of nigral dopaminergic cells: Indirect mediation through reticulata inhibitory neurons. Eur. J. Pharmacol., 59, 211-218.
22. Grace, A.A. & Bunney, B.S. (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience, 10, 301-315.
23. Grantyn, R. (1988) Gaze control through superior colliculus: Structure and function. In Buttner-Ennever, J.A. (Ed.), Neuroanatomy of the Oculomotor System. Elsevier, Amsterdam, pp. 273-333.
24. Guarraci, F.A. & Kapp, B.S. (1999) An electrophysiological characterization of ventral tegmental area dopaminergic neurons during differential Pavlovian fear conditioning in the awake rabbit. Behav. Brain Res., 99, 169-179.
25. Harting, J.K., Updyke, B.V. & Vanlieshout, D.P. (1992) Corticotectal projections in the cat - Anterograde transport studies of 25 cortical areas. J. Comp. Neurol., 324, 379-414.
26. Hebb, M.O. & Robertson, H.A. (2000) Identification of a subpopulation of substantia nigra pars compacta gamma-aminobutyric acid neurons that is regulated by basal ganglia activity. J. Comp. Neurol., 416, 30-44.
27. Horvitz, J.C. (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience, 96, 651-656.
28. Horvitz, J.C., Stewart, T. & Jacobs, B.L. (1997) Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res., 759, 251-258.
29. Hsu, S.M., Raine, L. & Fanger, H. (1981) The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase techniques. Am. J. Clin. Pathol., 75, 816-821.
30. Jay, M.F. & Sparks, D.L. (1987) Sensorimotor integration in the primate superior colliculus. I. Motor convergence. J. Neurophysiol., 57, 22-34.
31. Jessell, T.M., Emson, P.C., Paxinos, G. & Cuello, A.C. (1978) Topographic projections of substance P and GABA pathways in the striato- and pallidonigral system: a biochemical and immunohistochemical study. Brain Res., 152, 487-498.
32. Kakade, S. & Dayan, P. (2000) Dopamine bonuses. Neural Information Processing Systems, 12, 131-137.
33. Kiyatkin, E.A. (1988) Functional properties of presumed dopamine-containing and other ventral tegmental area neurones in conscious rats. Int. J. Neurosci., 42 , 21-43.
34. Kiyatkin, E.A. & Rebec, G.V. (1998) Heterogeneity of ventral tegmental area neurons: Single-unit recording and iontophoresis in awake, unrestrained rats. Neuroscience, 85, 1285-1309.
35. Kiyatkin, E.A. & Zhukov, V.N. (1988) Impulse activity of mesencephalic neurons on nociceptive stimulation in awake rats. Neurosci. Behav. Physiol., 18 , 393-400.
36. Krout, K.E., Loewy, A.D., Westby, G.W.M. & Redgrave, P. (2001) Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol., 431, 198-216.
37. Lee, P.H., Schmidt, M. & Hall, W.C. (2001) Excitatory and inhibitory circuitry in the superficial gray layer of the superior colliculus. J. Neurosci., 21, 8145-8153.
38. Lokwan, S.J.A., Overton, P.G., Berry, M.S. & Clark, D. (1999) Stimulation of the pedunculopontine tegmental nucleus in the rat produces burst firing in A9 dopaminergic neurons. Neuroscience, 92, 245-254.
39. Meredith, M.A. & Ramoa, A.S. (1998) Intrinsic circuitry of the superior colliculus: Pharmacophysiological identification of horizontally oriented inhibitory interneurons. J. Neurophysiol., 79, 1597-1602.
40. Nagai, T., McGeer, P.L. & McGeer, E.G. (1983) Distribution of GABA-T intensive neurons in the rat forebrain and midbrain. J. Comp. Neurol., 218, 220-238.
41. Naito, A. & Kita, H. (1994) The cortico-nigral projection in the rat - An anterograde tracing study with biotinylated dextran amine. Brain Res., 637, 317-322.
42. Niemi-Junkola, U.J. & Westby, G.W.M. (2000) Cerebellar output exerts spatially organized influence on neural responses in the rat superior colliculus. Neuroscience, 97, 565-573.
43. Overton, P.G. & Clark, D. (1997) Burst firing in midbrain dopaminergic neurons. Brain Res. Rev., 25, 312-334.
44. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney.
45. Prensa, L. & Parent, A. (2001) The nigrostriatal pathway in the rat: A single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J. Neurosci., 21, 7247-7260.
46. Redgrave, P., McHaffie, J.G. & Stein, B.E. (1996) Nociceptive neurones in rat superior colliculus, I. Antidromic activation from the contralateral predorsal bundle. Exp. Brain Res., 109, 185-196.
47. Redgrave, P. & Mitchell, I.J. (1982) Functional validation of projection topography in the nigrostriatal dopamine system. Neuroscience, 7, 885-894.
48. Redgrave, P., Mitchell, I.J. & Dean, P. (1987) Descending projections from the superior colliculus in rat: A study using orthograde transport of wheatgermagglutinin conjugated horseradish peroxidase. Exp. Brain Res., 68, 147-167.
49. Redgrave, P., Prescott, T.J. & Gurney, K. (1999) Is the short latency dopamine response too short to signal reward error? Trends Neurosci., 22, 146-151.
50. Redgrave, P., Simkins, M., Overton, P. & Dean, P. (1992) Anticonvulsant role of nigrotectal projection in the maximal electroshock model of epilepsy - I. Mapping of dorsal midbrain with bicuculline. Neuroscience, 46, 379-390.
51. Redgrave, P. & Westby, G.W.M. (1999) Does the superior colliculus play a role in the activation of dopamine cells by novel stimuli? Neurosci. Abstr., 25, 765.719.
52. Richards, C.D., Shiroyama, T. & Kitai, S.T. (1997) Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat. Neuroscience, 80, 545-557.
53. Robbins, T.W. & Everitt, B.J. (1996) Neurobehavioural mechanisms of reward and motivation. Curr. Opin. Neurobiol., 6, 228-236.
54. Salamone, J.D. (1994) The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav. Brain Res., 61, 117-133.
55. Schneider, G.E. (1969) Two visual systems. Science, 163, 895-901.
56. Schultz, W. (1998) Predictive reward signal of dopamine neurons. J. Neurophysiol., 80, 1-27.
57. Schultz, W., Dayan, P. & Montague, P.R. (1997) A neural substrate of prediction and reward. Science, 275, 1593-1599.
58. Schultz, W. & Dickinson, A. (2000) Neuronal coding of prediction errors. Annu. Rev. Neurosci., 23, 473-500.
59. Sesack, S.R. & Pickel, V.M. (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol., 320, 145-160.
60. Shehab, S., Coffey, P.J., Dean, P. & Redgrave, P. (1991) Regional expression of c-fos protein in rat brain following seizures induced by pentylenetetrazol (PTZ) or maximal electroshock (MES). Eur. J. Neurosci. Suppl., 4, 2036.
61. Smith, I.D. & Grace, A.A. (1992) Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse, 12, 287-303.
62. Sparks, D.L. (1986) Translation of sensory signals into commands for control of saccadic eye movements: Role of the primate superior colliculus. Physiol. Rev., 66, 118-171.
63. Steffensen, S.C., Svingos, A.L., Pickel, V.M. & Henriksen, S.J. (1998) Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J. Neurosci., 18, 8003-8015.
64. Stein, B.E. & Meredith, M.A. (1993) The Merging of the Senses. The MIT Press, Cambridge, MA.
65. Steinfels, G.F., Heym, J., Strecker, R.E. & Jacobs, B.L. (1983) Behavioral correlates of dopaminergic unit activity in freely moving cats. Brain Res., 258, 217-228.
66. Steriade, M. (2001) Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol., 86, 1-39.
67. Steriade, M., Nunez, A. & Amzica, F. (1993) A novel slow (less-than-1 hz) oscillation of neocortical neurons in-vivo - Depolarizing and hyperpolarizing components. J. Neurosci., 13, 3252-3265.
68. Suri, R.E. (2001) Anticipatory responses of dopamine neurons and cortical neurons reproduced by internal model. Exp. Brain Res., 140, 234-240.
69. Suri, R.E. & Schultz, W. (1999) A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience, 91, 871-890.
70. Telford, S., Wang, S. & Redgrave, P. (1996) Analysis of nociceptive neurones in the rat superior colliculus using c-fos immunohistochemistry. J. Comp. Neurol., 375, 601-617.
71. Tepper, J.M., Martin, L.P. & Anderson, D.R. (1995) GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J. Neurosci., 15, 3092-4103.
72. Thorpe, S.J. & Fabre-Thorpe, M. (2001) Seeking categories in the brain. Science, 291, 260-263.
73. Tokuno, H., Takada, M., Ikai, Y. & Mizuno, N. (1994) Direct projections from the deep layers of the superior colliculus to the subthalamic nucleus in the rat. Brain Res., 639, 156-160.
74. Tong, Z.Y., Overton, P.G. & Clark, D. (1996) Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events. Synapse, 22, 195-208.
75. Waddington, J.L. & Cross, A.J. (1980) The striatonigral GABA pathway: Functional and neurochemical characteristics in rats with unilateral striatal kainic acid lesions. Eur. J. Pharmacol., 67, 27-32.
76. Wang, S. & Redgrave, P. (1997) Microinjections of muscimol into lateral superior colliculus disrupt orienting and oral movements in the formalin model of pain. Neuroscience, 81, 967-988.
77. Wang, S., Wang, H., Niemi-Junkola, U., Westby, G.W.M., McHaffie, J.G., Stein, B.E. & Redgrave, P. (2000) Parallel analyses of nociceptive neurones in rat superior colliculus using c-fos immunohistochemistry and electrophysiology under different conditions of anaesthesia. J. Comp. Neurol., 425, 599-615.
78. Westby, G.W.M., Redgrave, P. & Dean, P. (1988) Electrophysiological characterisation of collicular output pathways mediating approach and avoidance in the rat. Neurosci. Lett. Suppl., 32, S39.
79. Wurtz, R.H. & Goldberg, M.E. (1972) The primate superior colliculus and the shift of visual attention. Invest. Ophthalmol., 11, 441-450.
80. Zhu, J.J. & Lo, F.S. (2000) Recurrent inhibitory circuitry in the deep layers of the rabbit superior colliculus. J. Physiol. (Lond.), 523, 731-740.