V,r,oo Rexarch. Vol. IX. pp. .3X7-W89 i: Pergmw~ Press Lid IY7X. Prmtcd in Great Brium
LETTER TO THE EDITORS
COMMENTS ON ORGANIZATIQN AND SPATIAL-FREQUENCY CHARACTERISTICS OF RECEPTIVE FIELDS IN THE VISUAL CORTEX (Receiced 22 Ju1.s 1977: in recised form 27 September 1977)
In a recent series of papers Schiller, Finlay and Volman (197&a,b) presented novel and interesting material concerning the organization and function of simple and complex receptive fields in the visual cortex. In this Letter we argue against two points in their conclusions. (1) Schiller et 01. (1976a, p. 1334) claim that both their S (simple) and CX (complex) cells work as narrow-band spatial frequency filters tuned solely to sinusoidal gratings, the selectivity to square-wave gratings being low. There is no need to stress the importance of this inference which. were it correct, would lead to a revision of the present concept as to the role of the Fourier analysis in description of the image by neurons of the visual cortex. We believe, however, that it is the stimulation procedure rather than the shape of a grating that was responsible for the inference in question. In the paper cited, a squarewave grating was passed through the receptive tieid at a constant translation velocity (T/set) whereas the velocity of a sinusoidal grating was varied so that the slits of the grating would cross the center of the field with the same temporal frequency (3.33 Hz). We took the spat~l-frequent characteristics with squarewave gratings moving at a constant velocity and the result was that the selectivity of neurons to squarewave gratings was equally good in 77”/; of neurons (Glezer, Ivanov and Tscherbach, 1973). It can be
I
shown, however, that even the neurons with poor selectivity are more selective when the relationship between the response and the spatial frequency is recorded in the same way as was carried out by Schiller er al. with sinusoidal gratings (Fig. 1A). This increase in selectivity is easy to explain by properties of the receptive fields as spatial-frequency filters. Tbe fieIds give a maximum response to a certain velocity of the grating. The higher the spatial frequency to which the field is tuned, the less is the optimum velocity (Fig. 2). Therefore it is only natural that with the introduction of an additional parameter-the variation of transiation velocity-the selectivity improves. It is of interest to note that the narrow bandwidth neurons fail to improve selectivity as the movement velocity is changed (Fig. 1B). (2) Our second objection concerns the weighting function of the complex tieids. Schiller er af. (1976b. Fig. 11, p. 1299) claim that the complex receptive fields consist of two homogeneous superimposed onand off-centers without inhibitory sidebands. The absence of inhibitory sidebands is inferred from the fact that a slit moving through a field does not inhibit the spontaneous discharges before entering the field. This is correct, as can be seen from Fig. 3(A). which shows the responses to the movement of slits of different widths through the field. The inference is wrong, however, for the inhibitory sidebands are readily
(A)
(9)
t
IOO-
c /deg Fig. I. The relationship between the response of a neuron in the visual cortex and spatial frequency of a grating passing its reaptive field at a constant translation velocity (triangles) and at a constant temporal frequency of slits crossing the center of field (circles). (A) Neuron 223-3, velocity C-,kec frequency 12.Ocisec. (B) Neuron 226-f. velocity 6’:‘sec. frequency 3.56 c’sec. 887
888
Letter to the Editors
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Fig. 1. Dependence of the characteristic of a receptive field on the velocity of a grating. (A) The distribution of the receptive fields over the optimum velocity of a grating; abscissa: the optimum velocity of movement: ordinate: the number of fields. {B) The width of optimum velocity ranges for three fields: abscissa: the velocity of a grating; ordinate: the response of a receptive field in arbitrary relat ive units.
f8f eldsq
revealed if judged by the evoked taneous)
(and not sponactivity (Glezer er al, 1973). When two slits
are moved through a geld. the response to the first slit is considerably weaker when the second slit enters the field via the inhibitory sideband. In this case the width of the second slit is critical for producing inhibition in the complex field, in contrast to the simple field. The response can be strongly inhibits when the width of a sfit is roughly equal (corresponds) to the width of the inhibitory sideband. For instance, the complete inhibition of the response to a grating 05 cideg is longer by loo0 msec than that to a grating 0.33 cideg, and after this period of comptete inhibition. the response is much weaker (Fig. 3B). From responses to single slits (Fig. 3A) and gratings of different spatial frequencies (shown partly in Fig. 3B) we can perform a reconstruction of the field. For
Fig. 3. Characteristics of a complex receptive field. (Af PSTH of responses to moving through the field of light slits of various widths (numbers on the right side). Each PSTH was obtained with I5 movements of a slit. The vertical solid lines are drawn through the dashes under the steps in PSTH. (B) The responses of a field (PSTH) to rectangular gratings of various spatial frequencies. Gratings width 6’. The peaks correspond to responses to gratings entering and leaving the fictd.
Letter to the Editors example 5 on-subfields, shown as solid vertical lines. are readily seen in Fig. 3(A) (see also Glezer et al.,
1973; Pollen and Ronner, 1975). It should be emphasized that it is such an organization consisting of several subfields that determines the properties of the complex receptive field as the spatial-frequency filter. It is unlikely that the differences under discussion are due to different animals used: we worked on cats and Schiller et ai. worked on monkeys. These authors themselves point to a great resemblance in the receptive fields of cats and monkeys with respect to their organization and occurrence. Again, it would be most strange if the concepts concerning the role of the receptive fields in the Fourier analysis of the image were applicable to the cat and man but not to the monkey. Pavlov Institute Academy
of Physiology of Sciences
of rhe Li.SS.R.
Leningrad, U.S.S.R.
V. D. GLEZER V. E. GAUZENAN T. A. TSHEREACH
K. N.
DUDKIN
889 REFERENCES
Glezer V. D., Ivanov V. A., Tscherbach T. A. (1973)Investigation of complex and hypercomplex receptive fields of visual cortex of the cat as spatial frequency filters. Vision
Rrs. 13. 18754904. Glezer V. D.. Cooperman A. M.. Ivanov V. A. and Tscher-
bath T. A. (1976) An investigation of spatial frequency characteristics of the complex receptive fields in the visual cortex of the cat. Vision Res. 16. 789-797. Pollen D. A.. Ronner S. F. (1975) Periodic excitabiiity changes across the receptive fields of complex ceils in the striate and parastriate cortex of the cat. J. PlrysioL. Land. 245. 667497.
Schiller P. H.. Finlay B. L. and Volman S. F. (1976a) Quantitative studies of single-cell properties in monkey striate cortex. III. Spatial frequency. J. NeurophysioL 39, 1334-1351. Schiller P. H.. Finlay B. L. and Volman S. F. (1976b) Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. J. ~~~r~ph~sjo~. 39. 1288-1319.
LETTER TO THE EDITORS
COMMENTS ON ORGANIZATIQN AND SPATIAL-FREQUENCY CHARACTERISTICS OF RECEPTIVE FIELDS IN THE VISUAL CORTEX (Receiced 22 Ju1.s 1977: in recised form 27 September 1977)
In a recent series of papers Schiller, Finlay and Volman (197&a,b) presented novel and interesting material concerning the organization and function of simple and complex receptive fields in the visual cortex. In this Letter we argue against two points in their conclusions. (1) Schiller et 01. (1976a, p. 1334) claim that both their S (simple) and CX (complex) cells work as narrow-band spatial frequency filters tuned solely to sinusoidal gratings, the selectivity to square-wave gratings being low. There is no need to stress the importance of this inference which. were it correct, would lead to a revision of the present concept as to the role of the Fourier analysis in description of the image by neurons of the visual cortex. We believe, however, that it is the stimulation procedure rather than the shape of a grating that was responsible for the inference in question. In the paper cited, a squarewave grating was passed through the receptive tieid at a constant translation velocity (T/set) whereas the velocity of a sinusoidal grating was varied so that the slits of the grating would cross the center of the field with the same temporal frequency (3.33 Hz). We took the spat~l-frequent characteristics with squarewave gratings moving at a constant velocity and the result was that the selectivity of neurons to squarewave gratings was equally good in 77”/; of neurons (Glezer, Ivanov and Tscherbach, 1973). It can be
I
shown, however, that even the neurons with poor selectivity are more selective when the relationship between the response and the spatial frequency is recorded in the same way as was carried out by Schiller er al. with sinusoidal gratings (Fig. 1A). This increase in selectivity is easy to explain by properties of the receptive fields as spatial-frequency filters. Tbe fieIds give a maximum response to a certain velocity of the grating. The higher the spatial frequency to which the field is tuned, the less is the optimum velocity (Fig. 2). Therefore it is only natural that with the introduction of an additional parameter-the variation of transiation velocity-the selectivity improves. It is of interest to note that the narrow bandwidth neurons fail to improve selectivity as the movement velocity is changed (Fig. 1B). (2) Our second objection concerns the weighting function of the complex tieids. Schiller er af. (1976b. Fig. 11, p. 1299) claim that the complex receptive fields consist of two homogeneous superimposed onand off-centers without inhibitory sidebands. The absence of inhibitory sidebands is inferred from the fact that a slit moving through a field does not inhibit the spontaneous discharges before entering the field. This is correct, as can be seen from Fig. 3(A). which shows the responses to the movement of slits of different widths through the field. The inference is wrong, however, for the inhibitory sidebands are readily
(A)
(9)
t
IOO-
c /deg Fig. I. The relationship between the response of a neuron in the visual cortex and spatial frequency of a grating passing its reaptive field at a constant translation velocity (triangles) and at a constant temporal frequency of slits crossing the center of field (circles). (A) Neuron 223-3, velocity C-,kec frequency 12.Ocisec. (B) Neuron 226-f. velocity 6’:‘sec. frequency 3.56 c’sec. 887
888
Letter to the Editors
05t
1632
248
4
n
Af -13.~-50k/~ie-g 2
aJl248t63.Z
I.
0
;I 0 E
9 cc
0
0
L
I
I
0.375
0.75
I.5
I
i
L
I
3.0
6.0
12
29
I
Y deg/sec
Fig. 1. Dependence of the characteristic of a receptive field on the velocity of a grating. (A) The distribution of the receptive fields over the optimum velocity of a grating; abscissa: the optimum velocity of movement: ordinate: the number of fields. {B) The width of optimum velocity ranges for three fields: abscissa: the velocity of a grating; ordinate: the response of a receptive field in arbitrary relat ive units.
f8f eldsq
revealed if judged by the evoked taneous)
(and not sponactivity (Glezer er al, 1973). When two slits
are moved through a geld. the response to the first slit is considerably weaker when the second slit enters the field via the inhibitory sideband. In this case the width of the second slit is critical for producing inhibition in the complex field, in contrast to the simple field. The response can be strongly inhibits when the width of a sfit is roughly equal (corresponds) to the width of the inhibitory sideband. For instance, the complete inhibition of the response to a grating 05 cideg is longer by loo0 msec than that to a grating 0.33 cideg, and after this period of comptete inhibition. the response is much weaker (Fig. 3B). From responses to single slits (Fig. 3A) and gratings of different spatial frequencies (shown partly in Fig. 3B) we can perform a reconstruction of the field. For
Fig. 3. Characteristics of a complex receptive field. (Af PSTH of responses to moving through the field of light slits of various widths (numbers on the right side). Each PSTH was obtained with I5 movements of a slit. The vertical solid lines are drawn through the dashes under the steps in PSTH. (B) The responses of a field (PSTH) to rectangular gratings of various spatial frequencies. Gratings width 6’. The peaks correspond to responses to gratings entering and leaving the fictd.
Letter to the Editors example 5 on-subfields, shown as solid vertical lines. are readily seen in Fig. 3(A) (see also Glezer et al.,
1973; Pollen and Ronner, 1975). It should be emphasized that it is such an organization consisting of several subfields that determines the properties of the complex receptive field as the spatial-frequency filter. It is unlikely that the differences under discussion are due to different animals used: we worked on cats and Schiller et ai. worked on monkeys. These authors themselves point to a great resemblance in the receptive fields of cats and monkeys with respect to their organization and occurrence. Again, it would be most strange if the concepts concerning the role of the receptive fields in the Fourier analysis of the image were applicable to the cat and man but not to the monkey. Pavlov Institute Academy
of Physiology of Sciences
of rhe Li.SS.R.
Leningrad, U.S.S.R.
V. D. GLEZER V. E. GAUZENAN T. A. TSHEREACH
K. N.
DUDKIN
889 REFERENCES
Glezer V. D., Ivanov V. A., Tscherbach T. A. (1973)Investigation of complex and hypercomplex receptive fields of visual cortex of the cat as spatial frequency filters. Vision
Rrs. 13. 18754904. Glezer V. D.. Cooperman A. M.. Ivanov V. A. and Tscher-
bath T. A. (1976) An investigation of spatial frequency characteristics of the complex receptive fields in the visual cortex of the cat. Vision Res. 16. 789-797. Pollen D. A.. Ronner S. F. (1975) Periodic excitabiiity changes across the receptive fields of complex ceils in the striate and parastriate cortex of the cat. J. PlrysioL. Land. 245. 667497.
Schiller P. H.. Finlay B. L. and Volman S. F. (1976a) Quantitative studies of single-cell properties in monkey striate cortex. III. Spatial frequency. J. NeurophysioL 39, 1334-1351. Schiller P. H.. Finlay B. L. and Volman S. F. (1976b) Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. J. ~~~r~ph~sjo~. 39. 1288-1319.
