The manner in which the nervous system allocates limited motor resources when confronted with conflicting behavioural demands is a crucial issue in understanding how sensory information is transformed into adaptive motor responses. Understanding this selection process is of particular concern in current models of functions of the basal ganglia1. Here we report that the basal ganglia use simultaneous enhancing and suppressing processes synergistically to modulate sensory activity in the superior colliculi, which are bilaterally paired midbrain structures involved in the control of visual orientation behaviours2. These complementary processes presumably ensure accurate gaze shifts mediated by the superior colliculi despite the presence of potential distractors.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Redgrave, P., Prescott, T. J. & Gurney, K. The basal ganglia: a vertebrate solution to the selection problem. Neuroscience 89, 1009–1023 (1999)
Stein, B. E. & Meredith, M. A. The Merging of the Senses (MIT Press, Cambridge, Massachusetts, 1993)
Lee, C., Rohrer, W. H. & Sparks, D. L. Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357–360 (1988)
Munoz, D. P. & Guitton, D. Tectospinal neurons in the cat have discharges coding gaze position error. Brain Res. 341, 184–188 (1985)
Chevalier, G., Vacher, S. & Deniau, J. M. Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behaviour. Exp. Brain Res. 53, 320–326 (1984)
Chevalier, G., Vacher, S., Deniau, J. M. & Desban, M. Disinhibition as a basic process in the expression of striatal function. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res. 334, 215–226 (1985)
Hikosaka, O. & Wurtz, R. H. Visual and oculomotor function of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J. Neurophysiol. 49, 1285–1301 (1983)
Joseph, J. P. & Boussaoud, D. Role of the cat substantia nigra pars reticulata in eye and head movements. 1. Neural activity. Exp. Brain Res. 57, 286–296 (1985)
Beckstead, R. M. A comparison of the intranigral disribution of nigrotectal neurons labelled with horseradish peroxidase in the monkey, cat and rat. J. Neurosci. 1, 121–125 (1981)
Harting, J. K., Huerta, M. F., Hashikawa, R., Weber, J. T. & Van Lieshout, D. P. Neuroanatomical studies of the nigrotectal projection in the cat. J. Comp. Neurol. 278, 615–631 (1988)
Chevalier, G., Thierry, A. M., Shibazaki, T. & Feger, J. Evidence for a GABAergic inhibitory nigrotectal pathway in the rat. Neurosci. Lett. 21, 67–70 (1981)
Karabelas, A. B. & Moschovakis, A. K. Nigral inhibitory termination of efferent neurons of the superior colliculus: an intracellar horseradish peroxidase study in the cat. J. Comp. Neurol. 239, 309–329 (1985)
May, P. J. & Hall, W. C. Relationships between the nigrotectal pathway and the cells of origin of the predorsal bundle. J. Comp. Neurol. 226, 357–376 (1984)
Chevalier, G. & Deniau, J. M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13, 277–280 (1990)
Wallace, S. F., Rosenquist, A. C. & Sprague, J. M. Ibotenic acid lesions of the lateral substantia nigra restore visual orientation behaviour in the hemianopic cat. J. Comp. Neurol. 296, 222–252 (1990)
Ryan, L. J. & Clark, K. B. The role of the subthalamic nucleus in the response of globus pallidus neurons to stimulation of the prelimbic and agranular frontal cortices in rats. Exp. Brain Res. 86, 641–651 (1991)
Kha, H. T. et al. Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: single axon reconstructions and immunohistochemical study. J. Comp. Neurol. 440, 20–30 (2001)
Mize, R. R., Luo, Q., Butler, G., Jeon, C. J. & Nabors, B. The calcium-binding proteins parvalbumin and calbindin-D 28K form complementary patterns in the cat superior colliculus. J. Comp. Neurol. 320, 243–256 (1992)
Kalesnykas, R. P. & Sparks, D. L. The interaction of visual and electrical activity of neurons in the monkey superior colliculus: Site and train characteristics affect saccade latency, amplitude and direction. Soc. Neurosci. Abstr. 25, 1920 (1999)
Wang, S. & Redgrave, P. Microinjections of muscimol into lateral superior colliculus disrupt orienting and oral movements in the formalin model of pain. Neuroscience 81, 967–988 (1997)
Infante, C. & Leiva, J. Simultaneous unitary neuronal activity in both superior colliculi and its relation to eye movements in the cat. Brain Res. 381, 390–392 (1986)
Behan, M. An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus in the cat. J. Comp. Neurol. 234, 105–116 (1985)
Mink, J. W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381–425 (1996)
Handel, A. & Glimcher, P. W. Contextual modulation of substantia nigra pars reticulata neurons. J. Neurophysiol. 83, 3042–3048 (2000)
Sato, M. & Hikosaka, O. Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement. J. Neurosci. 22, 2363–2373 (2002)
Alexander, G. E. & Crutcher, M. D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266–271 (1990)
Kita, H. & Kitai, S. T. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. Comp. Neurol. 260, 435–452 (1987)
Sprague, J. M. Interactions of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science 153, 1544–1547 (1966)
Wallace, S. F., Rosenquist, A. C. & Sprague, J. M. Recovery from cortical blindness mediated by destruction of nontectotectal fibres in the commissure of the superior colliculus in the cat. J. Comp. Neurol. 284, 429–450 (1989)
Karnath, H. O. New insights into the functions of the superior temporal cortex. Nature Rev. Neurosci. 2, 568–576 (2001)
We thank R. Coghill, P. Redgrave and T. Stanford for their critical comments on earlier versions of the manuscript, and N. London for editorial assistance. This work was supported by a grant from the National Institutes of Health to J.G.M. H.J. was partly supported by a grant from the National Institutes of Health to B.E.S.
The authors declare that they have no competing financial interests.
About this article
Cite this article
Jiang, H., Stein, B. & McHaffie, J. Opposing basal ganglia processes shape midbrain visuomotor activity bilaterally. Nature 423, 982–986 (2003). https://doi.org/10.1038/nature01698
Perturbation-driven paradoxical facilitation of visuo-spatial function: Revisiting the ‘Sprague effect’
Oculomotor control after hemidecortication: One hemisphere encodes normal ipsilateral oblique anti-saccades
European Journal of Neuroscience (2019)
Physiology International (2019)