Abstract
A neural model is constructed based on the structure of a visual orientation hypercolumn in mammalian striate cortex. It is then assumed that the perceived orientation of visual contours is determined by the pattern of neuronal activity across orientation columns. Using statistical estimation theory, limits on the precision of orientation estimation and discrimination are calculated. These limits are functions of single unit response properties such as orientation tuning width, response amplitude and response variability, as well as the degree of organization in the neural network. It is shown that a network of modest size, consisting of broadly orientation selective units, can reliably discriminate orientation with a precision equivalent to human performance. Of the various network parameters, the discrimination threshold depends most critically on the number of cells in the hypercolumn. The form of the dependence on cell number correctly predicts the results of psychophysical studies of orientation discrimination. The model system's performance is also consistent with psychophysical data in two situations in which human performance is not optimal. First, interference with orientation discrimination occurs when multiple stimuli activate cells in the same hypercolumn. Second, systematic errors in the estimation of orientation can occur when a stimulus is composed of intersecting lines. The results demonstrate that it is possible to relate neural activity to visual performance by an examination of the pattern of activity across orientation columns. This provides support for the hypothesis that perceived orientation is determined by the distributed pattern of neural activity. The results also encourage the view of neural activity. The results also are determined by the responses of many neurons rather than the sensitivity of individual cells.
Similar content being viewed by others
References
Andrews DP, Butcher AK, Buckley BR (1973) Acuities for spatial arrangement in line figures: human and ideal observers compared. Vision Res 13:599–620
Andriessen JJ, Bouma H (1976) Eccentric vision: adverse interactions between line segments. Vision Res 16:71–78
Blake R, Holopigian K (1985) Orientation selectivity in cats and humans assessed by masking. Vision Res 25:1459–1467
Blake R, Holopigian K, Jauch M (1985) Another visual illusion involving orientation. Vision Res 25:1469–1476
Blakemore C, Campbell FW (1969) On the existence in the human visual system of neurons selectivity sensitive to the orientation and size of retinal images. J Physiol 203:237–260
Blakemore C, Nachmias J (1971) The orientation selectivity of two visual after-effects. J Physiol 213:157–174
Blakemore C, Tobin EA (1972) Lateral inhibition between orientation detectors in the cat's visual cortex. Exp Brain Res 15:439–440
Blakemore C, Carpenter RHS, Georgeson MA (1970) Lateral inhibition between orientation detectors in the human visual system. Nature 228:37–39
Bouma H, Andriessen JJ (1970) Induced changes in the perceived orientation of line segments. Vision Res 10:333–349
Bradley A, Skottun BC, Ohzawa I, Sclar G, Freeman RD (1985) Neurophysiological evaluation of the differential response model for orientation and spatial-frequency discrimination. J Opt Soc Am A 2:1607–1610
Burns BD, Prichard R (1971) Geometrical illusions and the response of neurons in the cat's visual cortex to angle patterns. J Physiol 213:599–616
Campbell FW, Kulikowski JJ (1966) Orientational selectivity of the human visual system. J Physiol 187:437–445
Carpenter RHS, Blakemore C (1973) Interactions between orientations in human vision. Exp Brain Res 18:287–303
Cowey A, Rolls ET (1974) Human cortical magnification factor and its relation to visual acuity. Exp Brain Res 21:447–454
Cramer H (1946) Mathematical methods of statistics. Princeton University Press, Princeton
Creutzfeldt OD, kuhnt U, Benevento LA (1974) An intracellular analysis of visual cortical neurons response to moving stimuli: response in a cooperative neuronal network. Exp Brain Res 21:251–274
Daniel PM, Whitteridge D (1959) The representation of the visual field on the calcarine cortex in baboons and monkeys. J Physiol 148:33P
Daniel PM, Whitteridge D (1961) The representation of the visual field on the cerebral cortex in monkeys. J Physiol 159:203–221
Daniels JD, Pettigrew JD (1975) A study of inhibitory antagonism in cat visual cortex. Brain Res 93:41–62
Dean AF (1981) The variability of discharge of simple cells in the cat striate cortex. Exp Brain Res 44:437–440
De Valois RL, Yund EW, Hepler N (1982) The orientation and direction selectivity of cells in macaque visual cortex. Vision Res 22:531–544
Dow BM, Snyder AZ, Vautin RG, Bauer R (1981) Magnification factor and receptive field size in foveal striate cortex of the monkey. Exp Brain Res 44:213–228
Drasdo N (1977) The neural representation of visual space. Nature 266:554–556
Ferster D (1986) Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J Neurosci 6:1284–1301
Fisher RA (1925) Theory of statistical estimation. Proc Cambridge Philos Soc 22:700
Fries W, Albus K, Creutzfeldt OD (1977) Effects of interacting visual patterns on single cell responses in cats striate cortex. Vision Res 17:1001–1008
Ganz L (1966) Mechanism of the figural aftereffects. Psychol Rev 73:128–150
Heggelnd P, Albus K (1978) Response variability and orientation discrimination of single cells in striate cortex of cat. Exp Brain Res 32:197–211
Henry GH, Dreher B, Bishop PO (1974) Orientation specificity of cells in cat striate cortex. J Neurophysiol 37:1394–1409
Hitchcock B, Hickey T (1980) Ocular dominance columns: evidence for their presence in humans. Brain Res 182:176–179
Hotopf WHN, Ollerearnshaw C (1972) The regression to right angles tendency and the Poggendorf illusion. Br J Psychol 63:359–367
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. J Physiol 160:106–154
Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195:215–243
Hubel DH, Wiesel TN (1974a) Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol 158:267–293
Hubel DH, Wiesel TN (1974b) Uniformity of monkey striate cortex: a parallel relationship between field size, scatter, and magnification factor. J Comp Neurol 158:295–305
Hubel DH, Wiesel TN, Stryker MP (1978) Anatomical demonstration of orientation columns in macaque monkey. J Comp Neurol 177:361–380
Kan PLE van, Scobey RP, Gabor AJ (1985) Response covariance in cat visual cortex. Exp Brain Res 60:559–563
Kulikowski JJ, Abadi R, King-Smith PE (1973) Orientational selectivity of grating and line detectors in human vision. Vision Res 13:1479–1486
LeVay S, Connolly M, Houde J, Van Essen DC (1985) The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. J Neurosci 5:486–501
Levi DM, Klein SA, Aitsebaomo AP (1985) Vernier acuity, crowding, and cortical magnification. Vision Res 25:963–977
Movshon JA, Blakemore C (1973) Orientation specificity and spatial selectivity in human vision. Perception 2:53–60
Nelson JI, Frost BJ (1978) Orientation-selective inhibition from beyond the classical visual receptive field. Brain Res 139:359–365
Nelson JI, Kato H, Bishop PO (1977) Discrimination of orientation and position disparities by binocularly activated neurons in cat striate cortex. J Neurophysiol 40:260–283
O'Kusky J, Colonnier M (1982) A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys. J Comp Neurol 210:278–290
Orban GA (1984) Neuronal operations in the visual cortex. Springer, Berlin Heidelberg New York
Paradiso MA, Carney T (1986) Orientation discrimination as a function of stimulus eccentricity and size: nasal/temporal retinal asymmetry. Invest Ophthalmol Vis Sci 27:344
Penfield W, Rasmussen T (1950) The cerebral cortex of man: a clinical study of localization of function. Macmillan, New York
Phillips GC, Wilson HR (1984) Orientation bandwidths of spatial mechanisms measured by masking. J Opt Soc Am A1:226–232
Rose D (1979) An analysis of the variability of unit activity in the cat's visual cortex. Exp Brain Res 37:595–604
Rose D, Blakemore C (1974) An analysis of orientation selectivity in the cat's visual cortex. Exp Brain Res 20:1–17
Schiller PH, Finlay BL, Volman SF (1976a) Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. J Neurophysiol 39:1320–1333
Schiller PH, Finlay BL, Volman SF (1976b) Short-term response variability of monkey striate neurons. Brain Res 105:347–349
Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurons in the striate cortex of the cat. J Physiol 250:305–329
Talbot SA, Marshall WH (1941) Physiological studies on neural mechanisms of visual localizations and discrimination. Am J Ophthalmol 24:1255–1263
Thomas JP, Gille J (1979) Bandwidths of orientation channels in human vision. J Opt Soc Am 69:652–660
Thomas JP, Shimamura KK (1975) Inhibitory interactions between visual pathways tuned to different orientations. Vision Res 15:1373–1380
Tolhurst DJ, Thompson PG (1975) Orientation illusions and after-effects: inhibition between channels. Vision Res 15:967–972
Tolhurst DJ, Movshon JA, Dean AF (1983) The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23:775–785
Trees HL Van (1968) Detection, estimation, and modulation theory. Wiley, New York
Vandenbussche E, Orban GA (1983) Meridional variations in the line orientation discrimination of the cat. Behav Brain Res 9:237–255
Virsu V, Taskinen H (1975) Central inhibitory interactions in human vision. Exp Brain Res 23:65–74
Wallace GK, Crampin DJ (1969) The effct of background density on the Zollner illusion. Vision Res 9:167–177
Watkins DM, Berkley MA (1974) The orientation selectivity of single neurons in cat striate cortex. Exp Brain Res 19:433–446
Weintraub DJ, Virsu V (1972) Estimating the vertex of converging lines: angle misperception? Percept Psychophys 11:277–283
Westheimer G, Shimamura K, McKee SP (1976) Interference with line-orientation sensitivity. J Opt Soc Am 66:332–338
Wilson JR, Sherman SM (1976) Receptive-field characteristics of neurons in cat striate cortex: changes with visual field eccentricity. J Neurophysiol 39:512–533
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Paradiso, M.A. A theory for the use of visual orientation information which exploits the columnar structure of striate cortex. Biol. Cybern. 58, 35–49 (1988). https://doi.org/10.1007/BF00363954
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00363954