Abstract
Numerous brain regions encode variables using spatial distribution of activity in neuronal maps. Their specific geometry is usually explained by sensory considerations only. We provide here, for the first time, a theory involving the motor function of the superior colliculus to explain the geometry of its maps. We use six hypotheses in accordance with neurobiology to show that linear and logarithmic mappings are the only ones compatible with the generation of saccadic motor command. This mathematical proof gives a global coherence to the neurobiological studies on which it is based. Moreover, a new solution to the problem of saccades involving both colliculi is proposed. Comparative simulations show that it is more precise than the classical one.
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References
Anderson R, Keller E, Gandhi N, Das S (1998) Two-dimensional saccade-related population activity in superior colliculus in monkey. J Neurophysiol 80(2):798–817
Arai K, Keller E, Edelman J (1994) Two-dimensional neural network model of the primate saccadic system. Neural Netw 7:1115–1135
Arai K, Das S, Keller E, Aiyoshi E (1999) A distributed model of the saccade system: simulations of temporally perturbed saccades using position and velocity feedback. Neural Netw 12(10):1359–1375
Badler J, Keller E (2002) Decoding of a motor command vector from distributed activity in superior colliculus. Biol Cybern 86(3): 179–189
Bourbaki N (1972) Groupes et algèbres de Lie, Chapitres 2 et 3. Dunod, Paris
Dräger U, Hugel D (1976) Topography of visual and somatosensory projections to mouse superior colliculus. J Neurophysiol 39:91–101
Feldon S, Feldon P, Kruger L (1970) Topography of the retinal projection upon the superior colliculus of the cat. Vision Res 10:135–143
Girard B, Berthoz A (2005) From brainstem to cortex: computational models of saccade generation circuitry. Prog Neurobiol 77:215–251
van Gisbergen J, van Opstal A, Tax A (1987) Collicular ensemble coding of saccades based on vector summation. Neuroscience 21(2):541–555
Goffart L, Pélisson D (1998) Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria. J Neurophysiol 79:1942–1958
Goossens H, van Opstal A (2000) Blink-perturbed saccades in monkey. II. superior colliculus activity. J Neurophysiol 83:3430–3452
Goossens H, van Opstal A (2006) Dynamic ensemble coding of saccades in the monkey superior colliculus. J Neurophysiol 95:2326–2341
Grantyn A, Moschovakis A (2003) Structure–function relationships in the superior colliculus of higher mammals. In: Hall W, Moschovakis V (eds) The superior colliculus: new approaches for studying sensorimotor integration, methods & new frontiers in neuroscience, chap 5. CRC Press, Boca Raton, pp 107–145
Grantyn A, Brandi AM, Dubayle D, Graf W, Ugolini G, Hadjidimitrakis K, Moschovakis A (2002) Density gradients of trans-synaptically labeled collicular neurons after injections of rabbies virus in the lateral rectus muscle of the rhesus monkey. J Comp Neurol 451:346–361
Groh J (2001) Converting neural signals from place codes to rate codes. Biol Cybern 85(3):159–165
Herrero L, Rodríguez F, Salas C, Torres B (1998) Tail and eye movememnts evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120:291–05
Hirsch H (1976) Differential topology. Springer, New York
Hörmander L (1983) The Analysis of linear partial differential operators I. No 256. In: Grundlehren der mathematischen Wissenschaften. Springer, Berlin
Iwamoto Y, Yoshida K (2002) Saccadic dysmetria following inactivation of the primate fastigial oculomotor region. Neurosci Lett 325:211–215
Kaneko C, Evinger C, Fuchs A (1981) Role of the cat pontine burst neurons in generation of saccadic eye movements. J Neurophysiol 46(3):387–408
Keller E (1974) Participation of medial pontine reticular formation in eye movement generation in monkey. J Neurophysiol 37(2): 316–332
King W, Fuchs F (1979) Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. J Neurophysiol 42(3): 861–876
Knudsen E (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2(9):1177–1194
Lee C, Rohrer W, Sparks D (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332: 357–360
McIlwain J (1976) Large receptive fields and spatial transformations in the visual system. In: Porter R (eds) Neurophysiology II, Int Rev Physiol, vol 10. University Park Press, Baltimore, pp 223–248
McIlwain J (1983) Representation of the visual streak in visuotopic maps of the cat’s superior colliculus: influence of the mapping variable. Vision Res 23(5):507–516
Moschovakis A, Kitama T, Dalezios Y, Petit J, Brandi A, Grantyn A (1998) An anatomical substrate for the spatiotemporal transformation. J Neurosci 18(23):10219–10229
Munoz D, Waitzman D, Wurtz R (1996) Activity of neurons in monkey superior colliculus during interrupted saccades. J Neurphysiol 75(6):2562–2580
Olivier E, Porter J, May P (1998) Comparison of the distribution and somatodendritic morphology of tectotecal neurons in the cat and monkey. Vis Neurosci 15:903–922
van Opstal A, van Gisbergen J (1989) A nonlinear model for collicular spatial interactions underlying the metrical properties of electrically elicited saccades. Biol Cybern 60(3):171–183
Optican L (2005) Sensorimotor transformation for visually guided saccades. Ann NY Acad Sci 1039:132–148
Ottes F, van Gisbergen JA, Eggermont J (1986) Visuomotor fields of the superior colliculus: a quantitative model. Vision Res 26(6): 857–873
Robinson D (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808
Rosa M, Schmid L (1994) Topography and extent of visual-field representation in the superior colliculus of the megachiropteran Pteropus. Vis Neurosci 11:1037–1057
Schwarz E (1980) Computational anatomy and functional architecture of striate cortex: a spatial mapping approach to perceptual coding. Vision Res 20:645–669
Siminoff R, Schwassmann H, Kruger L (1966) An electrophysiological study of the visual projection to the superior colliculus of the rat. J Comp Neurol 127:435–444
Soetedjo R, Kaneko C, Fuchs A (2000) Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. J Neurophysiol 87:679–695
Sparks D, Holland R, Guthrie B (1976) Size and distribution of movement fields in the monkey superior colliculus. Brain Res 113:21–34
Yoshida K, McCrea R, Berthoz A, Vidal P (1982) Morphological and physiological characteristics of inhibitory burst neurons controlling horizontal rapid eye movements in the alert cat. J Neurophysiol 48(3):761–784
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This work is partly supported by the EU within the NEUROBOTICS integrated Project (The fusion of NEUROscience and roBOTICS, FP6-IST-FET-2003no. 001917).
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Tabareau, N., Bennequin, D., Berthoz, A. et al. Geometry of the superior colliculus mapping and efficient oculomotor computation. Biol Cybern 97, 279–292 (2007). https://doi.org/10.1007/s00422-007-0172-2
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DOI: https://doi.org/10.1007/s00422-007-0172-2