A direct projection from superior colliculus to substantia nigra for detecting salient visual events

Midbrain dopaminergic neurons respond to unexpected and biologically salient events, but little is known about the sensory systems underlying this response. Here we describe, in the rat, a direct projection from a primary visual structure, the midbrain superior colliculus (SC), to the substantia nigra pars compacta (SNc) where direct synaptic contacts are made with both dopaminergic and non-dopaminergic neurons. Complementary electrophysiological data reveal that short-latency visual responses in the SNc are abolished by ipsilateral lesions of the SC and increased by local collicular stimulation. These results show that the tectonigral projection is ideally located to relay short-latency visual information to dopamine-containing regions of the ventral midbrain. We conclude that it is within this afferent sensory circuitry that the critical perceptual discriminations that identify stimuli as both unpredicted and biologically salient are made.

[1]  T. Curran,et al.  Expression of c-fos protein in brain: metabolic mapping at the cellular level. , 1988, Science.

[2]  G. Chevalier,et al.  Honeycomb-like structure of the intermediate layers of the rat superior colliculus: afferent and efferent connections , 2001, Neuroscience.

[3]  J. Horvitz.  Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

[4]  M. Goodale,et al.  Cortico-tectal and intertectal modulation of visual responses in the rat's superior colliculus , 1973, Experimental Brain Research.

[5]  P. Dean,et al.  Event or emergency? Two response systems in the mammalian superior colliculus , 1989, Trends in Neurosciences.

[6]  Peter Redgrave,et al.  Phasic activation of substantia nigra and the ventral tegmental area by chemical stimulation of the superior colliculus: an electrophysiological investigation in the rat , 2003, The European journal of neuroscience.

[7]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[8]  W. Schultz,et al.  Dopamine responses comply with basic assumptions of formal learning theory , 2001, Nature.

[9]  W. Willis,et al.  The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris‐leucoagglutinin study. II. Descending projections , 1995, The Journal of comparative neurology.

[10]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[11]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

[12]  Manuel Rodriguez,et al.  Compartmental organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat , 2000, The Journal of comparative neurology.

[13]  M. Wittmann,et al.  Time perception and temporal processing levels of the brain. , 1999, Chronobiology international.

[14]  R. Weinberg,et al.  A tetramethylbenzidine/tungstate reaction for horseradish peroxidase histochemistry. , 1991, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[15]  W. Willis,et al.  The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris‐leucoagglutinin study. I. Ascending projections , 1995, The Journal of comparative neurology.

[16]  S. Thorpe,et al.  Seeking Categories in the Brain , 2001, Science.

[17]  J. Horvitz,et al.  Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat , 1997, Brain Research.

[18]  A. Rosenquist,et al.  Disinhibition of the superior colliculus restores orienting to visual stimuli in the hemianopic field of the cat , 1997, The Journal of comparative neurology.

[19]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[20]  W. Schultz.  Getting Formal with Dopamine and Reward , 2002, Neuron.

[21]  M. Basso.  Cognitive Set and Oculomotor Control , 1998, Neuron.

[22]  R H Wurtz,et al.  The primate superior colliculus and the shift of visual attention. , 1972, Investigative ophthalmology.

[23]  David L. Sparks,et al.  Sensori-motor integration in the primate superior colliculus , 1991 .

[24]  S. Hsu,et al.  The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. , 1981, American journal of clinical pathology.

[25]  F. Guarraci,et al.  An electrophysiological characterization of ventral tegmental area dopaminergic neurons during differential pavlovian fear conditioning in the awake rabbit , 1999, Behavioural Brain Research.

[26]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[27]  P. Overton,et al.  Burst firing in midbrain dopaminergic neurons , 1997, Brain Research Reviews.

[28]  J. Grafman,et al.  The roles of the cerebellum and basal ganglia in timing and error prediction , 2002, The European journal of neuroscience.

[29]  J. Sprague,et al.  Interaction of Cortex and Superior Colliculus in Mediation of Visually Guided Behavior in the Cat , 1966, Science.

[30]  P. Dean,et al.  Functional architecture of rodent superior colliculus: relevance of multiple output channels. , 1993, Progress in brain research.

[31]  J. Bolam,et al.  Glutamate‐enriched Inputs from the Mesopontine Tegmentum to the Entopeduncular Nucleus in the Rat , 1996, The European journal of neuroscience.

[32]  I Kanno,et al.  CBF change evoked by somatosensory activation measured by laser-Doppler flowmetry: independent evaluation of RBC velocity and RBC concentration. , 1999, The Japanese journal of physiology.

[33]  Joe C. Adams,et al.  Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains. , 1992, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[34]  G. Schneider.  Two visual systems. , 1969, Science.

[35]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[36]  D. Sparks,et al.  Sensorimotor integration in the primate superior colliculus. I. Motor convergence. , 1987, Journal of neurophysiology.

[37]  T. Tsumori,et al.  Organization of projections from the medial agranular cortex to the superior colliculus in the rat: a study using anterograde and retrograde tracing methods , 2001, Brain Research.

[38]  B. Bunney,et al.  Firing properties of substantia nigra dopaminergic neurons in freely moving rats. , 1985, Life sciences.

[39]  B E Stein,et al.  Small lateral suprasylvian cortex lesions produce visual neglect and decreased visual activity in the superior colliculus , 1988, The Journal of comparative neurology.

[40]  Hagai Bergman,et al.  Stepping out of the box: information processing in the neural networks of the basal ganglia , 2001, Current Opinion in Neurobiology.