Abstract
The spatio-temporal frequency response profiles of 73 neurons located in the superficial, retino-recipient layers of the feline superior colliculus (SC) were investigated. The majority of the SC cells responded optimally to very low spatial frequencies with a mean of 0.1 cycles/degree (c/deg). The spatial resolution was also low with a mean of 0.31 c/deg. The spatial frequency tuning functions were either low-pass or band-pass with a mean spatial frequency bandwidth of 1.84 octaves. The cells responded optimally to a range of temporal frequencies between 0.74 cycles/s (c/s) and 26.41 c/s with a mean of 6.84 c/s. The majority (68%) of the SC cells showed band-pass temporal frequency tuning with a mean temporal frequency bandwidth of 2.4 octaves, while smaller proportions of the SC units displayed high-pass (19%), low-pass (8%) or broad-band (5%) temporal tuning. Most of the SC units exhibited simple spectral tuning with a single maximum in the spatio-temporal frequency domain, while some neurons were tuned for spatial or temporal frequencies or speed tuned. Further, we found cells excited by gratings moving at high temporal and low spatial frequencies and cells whose activity was suppressed by high velocity movement. The spatio-temporal filter properties of the SC neurons show close similarities to those of their retinal Y and W inputs as well as those of their inputs from the cortical visual motion detector areas, suggesting their common role in motion analysis and related behavioral actions.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-007-0908-1/MediaObjects/221_2007_908_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-007-0908-1/MediaObjects/221_2007_908_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-007-0908-1/MediaObjects/221_2007_908_Fig3_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-007-0908-1/MediaObjects/221_2007_908_Fig4_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-007-0908-1/MediaObjects/221_2007_908_Fig5_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-007-0908-1/MediaObjects/221_2007_908_Fig6_HTML.gif)
Similar content being viewed by others
References
Abramson BP, Chalupa LM (1988) Multiple pathways from the superior colliculus to the extrageniculate visual thalamus of the cat. J Comp Neurol 271:397–418
Barlow HB, Blakemore C, Pettigrew JD (1967) The neural mechanism of binocular depth discrimination. J Physiol (Lond) 193:327–342
Berardi N, Bisti S, Cattaneo A, Fiorentini A, Maffei L (1982) Correlation between the preferred orientation and spatial frequency of neurones in visual areas 17 and 18 of the cat. J Physiol (Lond) 323:603–618
Bergeron A, Guitton D (2001) The superior colliculus and its control of fixation behavior via projections to brainstem omnipause neurons. Prog Brain Res 134:97–107
Bergeron A, Tardif E, Lepore F, Guillemot JP (1998) Spatial and temporal matching of receptive field properties of binocular cells in area 19 of the cat. Neuroscience 86:121–134
Bishop PO, Kozak W, Vakkur GJ (1962) Some quantitative aspects of the cat’s eye: axis and plane of reference, visual field coordinates and optics. J Physiol (Lond) 163:466–502
Bisti S, Sireteanu RC (1976) Sensitivity to spatial frequency and contrast of visual cells in the cat superior colliculus. Vision Res 16:247–251
Bisti S, Carmignoto G, Galli L, Maffei L (1985) Spatial-frequency characteristics of neurones of area 18 in the cat: dependence on the velocity of the visual stimulus. J Physiol (Lond) 359:259–268
Burke W, Dreher B, Wang C (1998) Selective block of conduction in Y optic nerve fibres: significance for the concept of parallel processing. Eur J Neurosci 10:8–19
Campbell FW, Cooper GF, Enroth-Cugell C (1969) The spatial selectivity of the visual cells of the cat. J Physiol (Lond) 203:223–235
Casanova C (1993) Response properties of neurons in area 17 projecting to the striate-recipient zone of the cat’s lateralis posterior-pulvinar complex: comparison with cortico-tectal cells. Exp Brain Res 96:247–259
Clifford CW, Ibbotson MR (2003) Fundamental mechanisms of visual motion detection: models, cells and functions. Prog Neurobiol 68: 409–437
Crowder NA, Dawson MR, Wylie DR (2003) Temporal frequency and velocity-like tuning in the pigeon accessory optic system. J Neurophysiol 90:1829–1841
Dec K, Waleszczyk WJ, Wróbel A, Harutiunian-Kozak BA (2001) The spatial substructure of visual receptive fields in the cat’s superior colliculus. Arch Ital Biol 139:337–355
Di Stefano M, Morrone MC, Burr DC (1985) Visual acuity of neurones in the cat lateral suprasylvian cortex. Brain Res 331:382–385
Dreher B, Hoffmann KP (1973) Properties of excitatory and inhibitory regions in the receptive fields of single units in the cat’s superior colliculus. Exp Brain Res 16:333–353
Dreher B, Michalski A, Ho RH, Lee CW, Burke W (1993) Processing form and motion in area 21a of cat visual cortex. Vis Neurosci 10:93–115
Eggers HM, Blakemore C (1978) Physiological basis of anisometropic amblyopia. Science 201:264–267
Friend SM, Baker CL Jr (1993) Spatio-temporal frequency separability in area 18 neurons of the cat. Vision Res 33:1765–1771
Guitton D, Munoz DP (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. I. Identification, localization, and effects of behavior on sensory responses. J Neurophysiol 66:1605–1623
Harman HH (1976) Modern factor analysis (revised), 3rd edn. University of Chicago Press, Chicago
Hashemi-Nezhad M, Wang C, Burke W, Dreher B (2003) Area 21a of cat visual cortex strongly modulates neuronal activities in the superior colliculus. J Physiol (Lond) 550:535–552
Hicks TP, Stark CA, Fletcher WA (1986) Origins of afferents to visual suprageniculate nucleus of the cat. J Comp Neurol 246:544–554
Hoffmann KP, Dreher B (1973) The spatial organisation of the excitatory region of receptive fields in the cat’s superior colliculus. Exp Brain Res 16:354–370
Hoffmann KP, Distler C (1989) Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. J Neurophysiol 62:416–428
Ibbotson MR, Mark RF (1994) Wide-field nondirectional visual units in the pretectum: do they suppress ocular following of saccade-induced visual stimulation. J Neurophysiol 72:1448–1450
Ibbotson MR, Price NSC (2001) Spatiotemporal tuning of directional neurons in mammalian and avian pretectum: a comparison of physiological properties. J Neurophysiol 86:2621–2624
Ibbotson MR, Mark RF, Maddess TL (1994) Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the wallaby, Macropus eugenii. J Neurophysiol 72:2927–2943
Katoh YY, Benedek G (1995) Organization of the colliculo-suprageniculate pathway in the cat: a wheat germ agglutinin-horseradish peroxidase study. J Comp Neurol 352:381–397
Lünenburger L, Kleiser R, Stuphorn V, Miller LE, Hoffmann KP (2001) A possible role of the superior colliculus in eye-hand coordination. Prog Brain Res 134:109–125
Maffei L, Fiorentini A (1973) The visual cortex as a spatial frequency analyser. Vision Res 13:1255–1267
Mendola JD, Payne BR (1993) Direction selectivity and physiological compensation in the superior colliculus following removal of areas 17 and 18. Vis Neurosci 10:1019–1026
Merabet L, Minville K, Ptito M, Casanova C (2000) Responses of neurons in the cat posteromedial lateral suprasylvian cortex to moving texture patterns. Neuroscience 97:611–623
Mimeault D, Paquet V, Molotchnikoff S, Lepore F, Guillemot JP (2004) Disparity sensitivity in the superior colliculus of the cat. Brain Res 1010:87–94
Minville K, Casanova C (1998) Spatial frequency processing in posteromedial lateral suprasylvian cortex does not depend on the projections from the striate-recipient zone of the cat’s lateral posterior-pulvinar complex. Neuroscience 84:699–711
Morley JW, Vickery RM (1997) Spatial and temporal frequency selectivity of cells in area 21a of the cat. J Physiol (Lond) 501:405–413
Morrone MC, Di Stefano M, Burr DC (1986) Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat. J Neurophysiol 56:969–986
Movshon JA, Thompson ID, Tolhurst DJ (1978a) Spatial summation in the receptive fields of simple cells in the cat’s striate cortex. J Physiol (Lond) 283:53–77
Movshon JA, Thompson ID, Tolhurst DJ (1978b) Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat’s visual cortex. J Physiol (Lond) 283:101–120
Munoz DP, Guitton D (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. J Neurophysiol 66:1624–1641
Munoz DP, Wurtz RH (1993a) Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70:559–575
Munoz DP, Wurtz RH (1993b) Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J Neurophysiol 70:576–589
Nagy A, Eördegh G, Benedek G (2003) Spatial and temporal visual properties of single neurons in the feline anterior ectosylvian visual area. Exp Brain Res 151:108–114
Newsome WT, Gizzi MS, Movshon JA (1983) Spatial and temporal properties of neurons in macaque MT. Invest Opthalmol Vis Sci 24(suppl):106
Norita M, Mucke L, Benedek G, Albowitz B, Katoh Y, Creutzfeldt OD. (1986) Connections of the anterior ectosylvian visual area (AEV). Exp Brain Res 62:225–240
Norita M, Kase M, Hoshino K, Meguro R, Funaki S, Hirano S, McHaffie JG (1996) Extrinsic and intrinsic connections of the cat’s lateral suprasylvian visual area. Prog Brain Res 112:231–250
Ogasawara K, McHaffie JG, Stein BE (1984) Two visual corticotectal systems in cat. J Neurophysiol 52:1226–1245
Olson CR, Graybiel AM (1987) Ectosylvian visual area of the cat: location, retinotopic organization, and connections. J Comp Neurol 261:277–294
Ouellette BG, Minville K, Faubert J, Casanova C (2004) Simple and complex visual motion response properties in the anterior medial bank of the lateral suprasylvian cortex. Neuroscience 123:231–245
Peck CK, Baro JA (1997) Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets. Exp Brain Res 113:291–302
Perrone JA, Thiele A (2001) Speed skills: measuring the visual speed analyzing properties of primate MT neurons. Nat Neurosci 4:526–532
Perrone JA, Thiele A (2002) A model of speed tuning in MT neurons. Vision Res 42:1035–1051
Pettigrew JD, Cooper ML, Blasdel GG (1979) Improved use of tapetal reflection for eye-position monitoring. Invest Ophthalmol Vis Sci 18:490–495
Pinter RB, Harris LR (1981) Temporal and spatial response characteristics of the cat superior colliculus. Brain Res 207:73–94
Priebe NJ, Cassanello CR, Lisberger SG (2003) The neural representation of speed in macaque area MT/V5. J Neurosci 23:5650–5661
Priebe NJ, Lisberger SG, Movshon JA (2006) Tuning for spatiotemporal frequency and speed in directionally selective neurons of macaque striate cortex. J Neurosci 26:2941–2950
Rodieck RW, Pettigrew JD, Bishop PO, Nikara T (1967) Residual eye movements in receptive-field studies of paralyzed cats. Vis Res 7:107–110
Rowe MH, Cox JF (1993) Spatial receptive-field structure of cat retinal W cells. Vis Neurosci 10:765–779
Saul AB, Humphrey AL (1990) Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. J Neurophysiol 64:206–224
Saul AB, Humphrey AL (1992) Temporal-frequency tuning of direction selectivity in cat visual cortex. Vis Neurosci 8:365–372
Schiller PH, Tehovnik EJ (2001) Look and see: how the brain moves your eyes about. Prog Brain Res 134:127–142
Schneider GE (1969) Two visual systems. Science 163:895–902
Schoppmann A, Hoffmann KP (1979) A comparison of visual responses in two pretectal nuclei and in the superior colliculus of the cat. Exp Brain Res 35:495–510
Sireteanu R, Hoffmann KP (1979) Relative frequency and visual resolution of X- and Y-cells in the LGN of normal and monocularly deprived cats: interlaminar differences. Exp Brain Res 34:591–603
Sprague JM (1996) Neural mechanisms of visual orienting responses. Prog Brain Res 112:1–15
Stein BE, Meredith MA (1991) Functional organization of the superior colliculus. In: Leventhal AG (ed) The neural basis of visual function. In: Cronly-Dillon J (series ed) Vision and visual dysfunction, vol 4, Macmillan, London, pp 85–110
Stein BE, Jiang W, Wallace MT, Stanford TR (2001) Nonvisual influences on visual-information processing in the superior colliculus. Prog Brain Res 134:143–156
Sur M, Sherman SM (1982) Linear and nonlinear W-cells in C-laminae of the cat’s lateral geniculate nucleus. J Neurophysiol 47:869–884
Tardif E, Bergeron A, Lepore F, Guillemot JP (1996) Spatial and temporal frequency tuning and contrast sensitivity of single neurons in area 21a of the cat. Brain Res 716:219–223
Tardif E, Richer L, Bergeron A, Lepore F, Guillemot JP (1997) Spatial resolution and contrast sensitivity of single neurons in area 19 of split-chiasm cats: a comparison with primary visual cortex. Eur J Neurosci 9:1929–1939
Tardif E, Lepore F, Guillemot JP (2000) Spatial properties and direction selectivity of single neurons in area 21b of the cat. Neuroscience 97:625–634
Tolhurst DJ, Movshon JA (1975) Spatial and temporal contrast sensitivity of striate cortical neurones. Nature 257:674–675
Waleszczyk WJ, Wang C, Burke W, Dreher B (1999) Velocity response profiles of collicular neurons: parallel and convergent visual information channels. Neuroscience 93:1063–1076
Waleszczyk WJ, Nagy A, Eördegh G, Wypych M, Benedek G (2003a) Spatiotemporal frequency response profiles of single neurons in the cat’s superior colliculus. Acta Neurobiol Exp 63:255
Waleszczyk WJ, Nagy A, Eördegh G, Wypych M, Benedek G (2003b) Speed tuned cells in feline superior colliculus. Acta Neurobiol Exp 63(suppl):85
Waleszczyk WJ, Wang C, Benedek G, Burke W, Dreher B (2004) Motion sensitivity in cat’s superior colliculus: contribution of different visual processing channels to response properties of collicular neurons. Acta Neurobiol Exp 64:209–228
Wang C, Waleszczyk WJ, Benedek G, Burke W, Dreher B (2001) Convergence of Y and non-Y channels onto single neurons in the superior colliculi of the cat. Neuroreport 12:2927–2933
Wurtz RH, Albano JE (1980) Visual-motor function of the primate superior colliculus. Annu Rev Neurosci 3:189–226
Wylie DRW, Crowder NA (2000) The spatio-temporal properties of fast and slow neurons in the pretectal nucleus lentiformis mesencephali in pigeons. J Neurophysiol 84:2529– 2540
Zumbroich TJ, Blakemore C (1987) Spatial and temporal selectivity in the suprasylvian visual cortex of the cat. J Neurosci 7:482–500
Acknowledgments
We thank Zita Márkus and Alice Roxin, medical students at Albert Szent-Györgyi Medical and Pharmaceutical Center, for their participation in some of the experiments described here, Gabriella Dósai for her skilful technical assistance, and Péter Liszli for computer programming. Thanks are due to Prof. Bogdan Dreher and the reviewers for their helpful comments on the manuscript. The work was supported financially by the Polish State Committee for Scientific Research grant no. 3P04C08222, Hungarian OTKA grant no. T042610 and ETT grant no. 429/2003.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Waleszczyk, W.J., Nagy, A., Wypych, M. et al. Spectral receptive field properties of neurons in the feline superior colliculus. Exp Brain Res 181, 87–98 (2007). https://doi.org/10.1007/s00221-007-0908-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-007-0908-1