Neural Substrates of Sensory-guided Locomotor Decisions in the Rat Superior Colliculus

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2008 Oct 23

PMID 18940594

Citations 89

Authors

Gidon Felsen

Zachary F Mainen

Affiliations

Soon will be listed here.

Abstract

Deciding in which direction to move is a ubiquitous feature of animal behavior, but the neural substrates of locomotor choices are not well understood. The superior colliculus (SC) is a midbrain structure known to be important for controlling the direction of gaze, particularly when guided by visual or auditory cues, but which may play a more general role in behavior involving spatial orienting. To test this idea, we recorded and manipulated activity in the SC of freely moving rats performing an odor-guided spatial choice task. In this context, not only did a substantial majority of SC neurons encode choice direction during goal-directed locomotion, but many also predicted the upcoming choice and maintained selectivity for it after movement completion. Unilateral inactivation of SC activity profoundly altered spatial choices. These results indicate that the SC processes information necessary for spatial locomotion, suggesting a broad role for this structure in sensory-guided orienting and navigation.

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References

Robinson D . Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 1972; 12(11):1795-808. DOI: 10.1016/0042-6989(72)90070-3. View

Ingle D . Two visual systems in the frog. Science. 1973; 181(4104):1053-5. DOI: 10.1126/science.181.4104.1053. View

Mohler C, WURTZ R . Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. J Neurophysiol. 1976; 39(4):722-44. DOI: 10.1152/jn.1976.39.4.722. View

SCHILLER P, True S, CONWAY J . Deficits in eye movements following frontal eye-field and superior colliculus ablations. J Neurophysiol. 1980; 44(6):1175-89. DOI: 10.1152/jn.1980.44.6.1175. View

McHaffie J, Stein B . Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res. 1982; 247(2):243-53. DOI: 10.1016/0006-8993(82)91249-5. View

Redgrave P, Gurney K, Reynolds J . What is reinforced by phasic dopamine signals?. Brain Res Rev. 2007; 58(2):322-39. DOI: 10.1016/j.brainresrev.2007.10.007. View

Sparks D . Conceptual issues related to the role of the superior colliculus in the control of gaze. Curr Opin Neurobiol. 1999; 9(6):698-707. DOI: 10.1016/s0959-4388(99)00039-2. View

Hikosaka O, WURTZ R . Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. J Neurophysiol. 1985; 53(1):266-91. DOI: 10.1152/jn.1985.53.1.266. View

Ingle D, Crews D . Vertebrate neuroethology: definitions and paradigms. Annu Rev Neurosci. 1985; 8:457-94. DOI: 10.1146/annurev.ne.08.030185.002325. View

10.

Sparks D . Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol Rev. 1986; 66(1):118-71. DOI: 10.1152/physrev.1986.66.1.118. View

11.

Sahibzada N, Dean P, Redgrave P . Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci. 1986; 6(3):723-33. PMC: 6568468. View

12.

Jay M, Sparks D . Sensorimotor integration in the primate superior colliculus. I. Motor convergence. J Neurophysiol. 1987; 57(1):22-34. DOI: 10.1152/jn.1987.57.1.22. View

13.

Sinnamon H, Garcia E . Lateral neglect in a head movement task: more impairment with unilateral than bilateral lesions of the superior colliculus in the rat. Behav Brain Res. 1988; 27(2):131-43. DOI: 10.1016/0166-4328(88)90039-3. View

14.

Dean P, Mitchell I, Redgrave P . Contralateral head movements produced by microinjection of glutamate into superior colliculus of rats: evidence for mediation by multiple output pathways. Neuroscience. 1988; 24(2):491-500. DOI: 10.1016/0306-4522(88)90344-2. View

15.

Waitzman D, Ma T, Optican L, WURTZ R . Superior colliculus neurons provide the saccadic motor error signal. Exp Brain Res. 1988; 72(3):649-52. DOI: 10.1007/BF00250610. View

16.

Dean P, Redgrave P, Westby G . Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 1989; 12(4):137-47. DOI: 10.1016/0166-2236(89)90052-0. View

17.

Taube J, Muller R, RANCK Jr J . Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci. 1990; 10(2):420-35. PMC: 6570151. View

18.

Sparks D . The deep layers of the superior colliculus. Rev Oculomot Res. 1989; 3:213-55. View

19.

Glimcher P, Sparks D . Movement selection in advance of action in the superior colliculus. Nature. 1992; 355(6360):542-5. DOI: 10.1038/355542a0. View

20.

Weldon D, Best P . Changes in sensory responsivity in deep layer neurons of the superior colliculus of behaving rats. Behav Brain Res. 1992; 47(1):97-101. DOI: 10.1016/s0166-4328(05)80257-8. View