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Differences in direction specificity of receptive fields in upper and lower layers of the cat's prestriate area 18
Neuroscience Letters, 54 (1985) 59-63 Elsevier Scientific Publishers Ireland Ltd.
59
NSL 03139
DIFFERENCES IN DIRECTION SPECIFICITY OF RECEPTIVE FIELDS IN UPPER AND LOWER LAYERS OF THE CAT'S PRESTRIATE AREA 18
R. BAUER, M. MAYR and H.P. HUBER
Abteilung fiir Vergleichende Neurobiologie, Biologic IV. Universitiit Utili. Oberer Eselsberg, D-7900 utili (F.R.G.)
(Received October 16th, 1984; Revised version received and accepted November 16th, 1984)
Key words: direction specificity - area 18 - cortex - visual system - awake cats
Direction specificity was measured for neurons in area 18 (AI8) in penetrations approximately perpendicular to the layers in awake cats. A majority of lower layer cells (below 1.0 mm) preferred stimuli moving at rather orthogonal directions with respect to the preferred directions of the neurons in the upper layers (0-1.0 mm). The results suggest more functional autonomy of the corresponding cortical layers.
Preferred orientation is regarded as the typical constant parameter of the cells in a radial column across all cortical layers. This results from an amount of experiments which were led by Hubel and Wiesel's work on AI7 and AI8 of the cat [7, 8]. Preferred direction is orthogonal to the preferred orientation, and it is organized in column fashion at least in upper layers, too [12]. The constancy of the orientation parameter was weakened recently. In a series of systematic experiments with penetrations fairly parallel to the cortical layers both in monkey [3, 4, 9] and in cat [I, 2] a major orientation shift between upper and lower layers of striate cortex was found. The question arises, if this finding is a more general structural principle of prestriate cortex, too. As movement is a typical stimulus parameter for cells in AI8 [10, 11, 13], it seemed appropriate to answer this question by testing the directional preference of Al8 cells across the layers. The data presented here are from a study of AI8 cells during optokinetic nystagmus [6]. A detailed description of the stimulating and recording conditions is given there. The methods used for the histologic control are contained comprehensively in different reports [I, 2]. In brief: awake cats were stimulated with a moving large area Julesz-pattern along a circular path at 10-50° Is. All penetrations were localized in stereotaxic. coordinates between 1.5 and 4 mm in the lateral and between 0 and 7 mm in the anterior direction. Additional confirmation of AI8 cells came from physiological criteria [11] and cytoarchitectonic control. All results are presented in terms of directionality because preferred orientation cannot be deduced exactly from the directional preference measured by a large area noise pattern [5].
60
Thirty penetrations with 124 cells from 4 cats were selected on the criteria given above with 27 penetrations having 3 or more recording sites between 0 and 1.5 mm of depth which was relative to the position of the first stimulus-specific noise on the amplifier. Fig. lA, B shows the directionally tuned discharge frequency histograms, each from 4 cells in two different penetrations. Note the shift of the distribution peak below I mm of depth against the fairly constant peak position in the upper layer cells. Fig. l C shows the reconstruction of a penetration with 4 recording sites at different relative depths. The arrows indicate the preferred direction of the neurons. Note the rather orthogonal preferred directions at position 1/2 and 3/4 across the border of layers 4 and 5. The microphotograph of this histologic section is shown elsewhere [6]. To display all data in a comprehensive way, we chose to process them in the following way. The peak position of the histogram from the top cell in each penetration was set to zero and the difference of the directional axis of all following cells to the top cell was determined either clockwise or counterclockwise so t~at the maximal angle was at most 90 0 • To account for the directionality on the full 360 0 cycle, 4 symbols have been used to categorize the preferred directions according to the 4 quadrants of the inset in Fig. 2A. Bidirectional cells are represented by two values. If the top cell itself was bidirectional, the strongest peak was chosen as reference A 0.08
B
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Fig. I. Tuning curves for stimulus direction in two different penetrations (A, D) each one represented by 4 cells. The numbers on the left of each histogram represent the cortical depth, the ones on the right represent the maximal spike numbers per bin. Note the shift of the peaks around I mm of cortical depth. C: reconstruction of a penetration with 4 recording sites from a microsection. Position 4 was marked by a microlesion. The arrows indicate the preferred direction, the numbers on the right give the relative depth at each recording site.
61
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Fig. 2. A: deviation angles of the directional axis to the top cells' preferred direction for all successive cells in individual penetrations as a function of relative cortical depth. Different symbols represent different directional quadrants in the 3600 cycle. The crosses indicate the percentage of filled symbols in successive bins of 150I'm along the depth scale. B: distances of individual data points from the regression line filled 10 upper layer values of individual penetrations. Asterisks represent used data, dots represent data not used for calculating the regression lines. For details see text.
62
point. Only values between 0 and 1.5 mm of relative depth are used. Beyond of this depth the electrode often crossed the radial celI columns in the lower half of layer 6 at a too large angle, as verified in histologic controls. Fig. 2A shows alI normalized data as a function of the relative depth. In this plot the data are not folded back at the 90° line. According to the inset, two sets of data (quadrant 180 and 270) are reflected as a mirror image at the base line. Crosses indicate the absolute percentage increase of cells whose directional axis is different 45-90° from the axis of the top celI. By definition this angle cannot exceed 90°. In this cumulative plot it cannot be distinguished if this distribution is the sum of many single penetrations all with a continuous steep lateral drift or if it is due to neurons in lower layers with preferred directions rather orthogonal to the upper layer ones in the same columnar element. Most penetrations were not ideal penetrations. They showed deviations from the radial fiber course of up to 10-20° (see below). Such penetrations produce a tangential distance against the top point of 170-340 Jlm after I mm of penetration depth, enough to account for 45-90° of difference in preferred direction against the top celI. One can test this hypothesis by fitting regression lines in single penetrations to the upper layer values and by testing the predictability of the values in lower layers. The test was carried out on 14 penetrations with at least 3 measurements between o and 0.9 mm of depth. A regression line (least square fit) was fitted to these mostly upper layer values in Fig. 2A, and the distance of all measured values to the regression line was determined in each penetration. Fig. 2B shows the result. The asterisks represent values used for calculating the regression lines, and they are therefore with few exceptions of a constant smalI size. The dots represent values not used for the calculation of the regression line and they span the fulI range on the ordinate. This difference in data scatter along the extrapolated regression line is only obtained if the border between the two groups is set between 0.8 mm and I mm, i.e. it does not depend on the method as such. Therefore, if the selection of the 14 penetrations in Fig. 2B is representative, the distribution of Fig. 2A is most likely based on lower layer celIs with directional preferences rather orthogonal to the upper layer ones. AlIowing a predictability range of 0° to 45° in Fig. 2B, there is no or rather an 'inverse predictability' of 0.46 for the directional axis below of 0.9 mm. But if one accepts a scatter for upper layer cortical width and depth measurement between 0.8 mm and 1.2 mm (see below) the probability of lower layer celIs being 45-90° different from the expected value would approximate 600/0 or 70%. A representative amou'.lt of 15 penetration tracks has been identified by the use of lesions. On the average the electrodes deviated in the coronal plane from the course of the radial fibers by 8° (s = ± 5) on top and by 12° (s = ± 10) at the border between layers 4 and 5, in the sagittal plane less than 10°. This angle corresponds only to about 80 Jlm of tangential movement between 0.8 and 1.2 mm of depth and can therefore not account for the increase of preferred directions orthogonal to the upper layer values in Fig. 2A, B. The depth of 1 mm, correlated with the steep in-
63
crease of filled symbols in Fig. 2A, corresponds fairly well to the border of layers 4 and 5. A correction factor as the ratio of the histologic measurement (corrected for shrinkage) over the depth on the microdrive scale indicates the discrepancy between both measurements. This correction factor has been established in 26 histologically controlled penetrations in this and other studies [2] as 0.92 (S.D. ±O.I6), i.e. the microdrive readings overestimate the real depth by only 8% on the average. In summary, two conclusions are supported by the data. First, there is no predictability of infragranular preferred directions from the correspondent upper layer values. Second, there is at least a group of lower layer cells with preferred directions rather orthogonal to the correspondent parameter in upper layers. This group seems not to be a small minority, and it therefore consists not only of interneurons but it includes efferent principal neurons, too. The results from AI8 arc similar to the corresponding results from AI? [I, 2]. The functional significance of the shift phenomenon is far from being understood, but it suggests a relative functional autonomy of upper and lower layers as discussed already [2] for the striate area. I Bauer, R., A high probability of an orientation shift between layers 4 and 5 in central parts of the cat striate cortex, Exp. Brain Res., 48 (1982) 245-255. 2 Bauer, R., Differences in orientation and receptive field position between supra- and infragranular cells of cat striate cortex and their possible functional implications, BioI. Cybern., 49 (1983) 137-148. 3 Bauer, R., Dow, B.M. and Vautin, R.O., Laminar distribution of preferred orientations in foveal striate cortex of the monkey, Exp. Brain Res., 41 (1980) 54-60. 4 Bauer, R., Dow, B.M., Snyder, A.Z. and Vautin, R.O., Orientation shift between upper and lower layers in monkey visual cortex, Exp. Brain Res., 50 (1983) 133-145. 5 Hammond, P., Directional tuning of complex cells in area 17 of the feline visual cortex, J. Physiol. (Lond.), 285 (1978) 479-491. 6 Hoffmann, K.-P., Bauer, R., Huber, H.P. and Mayr, 1\1., Single cell activity in area 18 of the eat's visual cortex during optokinetic nystagmus, Exp. Brain Res., 57 (1984) 118-127. 7 Hubel, D.H. and Wiesel, T.N., Receptive fields, binocular interaction, and functional architecture in the eat's visual cortexv J,' Physiol. (Lond.), 160 (1962) 106-157. 8 Hubel, D.H. and Wiesel, T.N., Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. 9 Krueger, J. and Bach, M., Independent systems of orientation columns in upper and lower layers of monkey visual cortex, Neurosci. Lett., 31 (1982) 225-230. 10 Movshon, J.A., Thomson, 1.0. and Tolhurst, D.J. Spatial and temporal contrast sensitivity of neurons in area 17 and 18 of the cats' visual cortex, J. Physiol. (Lond.), 283 (1978) 101-120. II Orban, O.A., Kennedy, H. and Maes, H., Response to movement of neurons in area 17 and 18 of the cat: velocity sensitivity, J. Neurophysiol., 45 (1981) 1043-1058. 12 Tolhurst, D.J., Dean, A.F. and Thomson, 1.0., Preferred direction of movement as an element in the organization of cat visual cortex, Exp. Brain Res., 44 (1981) 340-342. 13 Tretter, F., Cynader, 1\1. and Singer, W., Cat parastriate cortex: a primary or secondary visual area? J. Neurophysiol., 38 (1975) 1099-1113.
59
NSL 03139
DIFFERENCES IN DIRECTION SPECIFICITY OF RECEPTIVE FIELDS IN UPPER AND LOWER LAYERS OF THE CAT'S PRESTRIATE AREA 18
R. BAUER, M. MAYR and H.P. HUBER
Abteilung fiir Vergleichende Neurobiologie, Biologic IV. Universitiit Utili. Oberer Eselsberg, D-7900 utili (F.R.G.)
(Received October 16th, 1984; Revised version received and accepted November 16th, 1984)
Key words: direction specificity - area 18 - cortex - visual system - awake cats
Direction specificity was measured for neurons in area 18 (AI8) in penetrations approximately perpendicular to the layers in awake cats. A majority of lower layer cells (below 1.0 mm) preferred stimuli moving at rather orthogonal directions with respect to the preferred directions of the neurons in the upper layers (0-1.0 mm). The results suggest more functional autonomy of the corresponding cortical layers.
Preferred orientation is regarded as the typical constant parameter of the cells in a radial column across all cortical layers. This results from an amount of experiments which were led by Hubel and Wiesel's work on AI7 and AI8 of the cat [7, 8]. Preferred direction is orthogonal to the preferred orientation, and it is organized in column fashion at least in upper layers, too [12]. The constancy of the orientation parameter was weakened recently. In a series of systematic experiments with penetrations fairly parallel to the cortical layers both in monkey [3, 4, 9] and in cat [I, 2] a major orientation shift between upper and lower layers of striate cortex was found. The question arises, if this finding is a more general structural principle of prestriate cortex, too. As movement is a typical stimulus parameter for cells in AI8 [10, 11, 13], it seemed appropriate to answer this question by testing the directional preference of Al8 cells across the layers. The data presented here are from a study of AI8 cells during optokinetic nystagmus [6]. A detailed description of the stimulating and recording conditions is given there. The methods used for the histologic control are contained comprehensively in different reports [I, 2]. In brief: awake cats were stimulated with a moving large area Julesz-pattern along a circular path at 10-50° Is. All penetrations were localized in stereotaxic. coordinates between 1.5 and 4 mm in the lateral and between 0 and 7 mm in the anterior direction. Additional confirmation of AI8 cells came from physiological criteria [11] and cytoarchitectonic control. All results are presented in terms of directionality because preferred orientation cannot be deduced exactly from the directional preference measured by a large area noise pattern [5].
60
Thirty penetrations with 124 cells from 4 cats were selected on the criteria given above with 27 penetrations having 3 or more recording sites between 0 and 1.5 mm of depth which was relative to the position of the first stimulus-specific noise on the amplifier. Fig. lA, B shows the directionally tuned discharge frequency histograms, each from 4 cells in two different penetrations. Note the shift of the distribution peak below I mm of depth against the fairly constant peak position in the upper layer cells. Fig. l C shows the reconstruction of a penetration with 4 recording sites at different relative depths. The arrows indicate the preferred direction of the neurons. Note the rather orthogonal preferred directions at position 1/2 and 3/4 across the border of layers 4 and 5. The microphotograph of this histologic section is shown elsewhere [6]. To display all data in a comprehensive way, we chose to process them in the following way. The peak position of the histogram from the top cell in each penetration was set to zero and the difference of the directional axis of all following cells to the top cell was determined either clockwise or counterclockwise so t~at the maximal angle was at most 90 0 • To account for the directionality on the full 360 0 cycle, 4 symbols have been used to categorize the preferred directions according to the 4 quadrants of the inset in Fig. 2A. Bidirectional cells are represented by two values. If the top cell itself was bidirectional, the strongest peak was chosen as reference A 0.08
B
12
18
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Fig. I. Tuning curves for stimulus direction in two different penetrations (A, D) each one represented by 4 cells. The numbers on the left of each histogram represent the cortical depth, the ones on the right represent the maximal spike numbers per bin. Note the shift of the peaks around I mm of cortical depth. C: reconstruction of a penetration with 4 recording sites from a microsection. Position 4 was marked by a microlesion. The arrows indicate the preferred direction, the numbers on the right give the relative depth at each recording site.
61
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Fig. 2. A: deviation angles of the directional axis to the top cells' preferred direction for all successive cells in individual penetrations as a function of relative cortical depth. Different symbols represent different directional quadrants in the 3600 cycle. The crosses indicate the percentage of filled symbols in successive bins of 150I'm along the depth scale. B: distances of individual data points from the regression line filled 10 upper layer values of individual penetrations. Asterisks represent used data, dots represent data not used for calculating the regression lines. For details see text.
62
point. Only values between 0 and 1.5 mm of relative depth are used. Beyond of this depth the electrode often crossed the radial celI columns in the lower half of layer 6 at a too large angle, as verified in histologic controls. Fig. 2A shows alI normalized data as a function of the relative depth. In this plot the data are not folded back at the 90° line. According to the inset, two sets of data (quadrant 180 and 270) are reflected as a mirror image at the base line. Crosses indicate the absolute percentage increase of cells whose directional axis is different 45-90° from the axis of the top celI. By definition this angle cannot exceed 90°. In this cumulative plot it cannot be distinguished if this distribution is the sum of many single penetrations all with a continuous steep lateral drift or if it is due to neurons in lower layers with preferred directions rather orthogonal to the upper layer ones in the same columnar element. Most penetrations were not ideal penetrations. They showed deviations from the radial fiber course of up to 10-20° (see below). Such penetrations produce a tangential distance against the top point of 170-340 Jlm after I mm of penetration depth, enough to account for 45-90° of difference in preferred direction against the top celI. One can test this hypothesis by fitting regression lines in single penetrations to the upper layer values and by testing the predictability of the values in lower layers. The test was carried out on 14 penetrations with at least 3 measurements between o and 0.9 mm of depth. A regression line (least square fit) was fitted to these mostly upper layer values in Fig. 2A, and the distance of all measured values to the regression line was determined in each penetration. Fig. 2B shows the result. The asterisks represent values used for calculating the regression lines, and they are therefore with few exceptions of a constant smalI size. The dots represent values not used for the calculation of the regression line and they span the fulI range on the ordinate. This difference in data scatter along the extrapolated regression line is only obtained if the border between the two groups is set between 0.8 mm and I mm, i.e. it does not depend on the method as such. Therefore, if the selection of the 14 penetrations in Fig. 2B is representative, the distribution of Fig. 2A is most likely based on lower layer celIs with directional preferences rather orthogonal to the upper layer ones. AlIowing a predictability range of 0° to 45° in Fig. 2B, there is no or rather an 'inverse predictability' of 0.46 for the directional axis below of 0.9 mm. But if one accepts a scatter for upper layer cortical width and depth measurement between 0.8 mm and 1.2 mm (see below) the probability of lower layer celIs being 45-90° different from the expected value would approximate 600/0 or 70%. A representative amou'.lt of 15 penetration tracks has been identified by the use of lesions. On the average the electrodes deviated in the coronal plane from the course of the radial fibers by 8° (s = ± 5) on top and by 12° (s = ± 10) at the border between layers 4 and 5, in the sagittal plane less than 10°. This angle corresponds only to about 80 Jlm of tangential movement between 0.8 and 1.2 mm of depth and can therefore not account for the increase of preferred directions orthogonal to the upper layer values in Fig. 2A, B. The depth of 1 mm, correlated with the steep in-
63
crease of filled symbols in Fig. 2A, corresponds fairly well to the border of layers 4 and 5. A correction factor as the ratio of the histologic measurement (corrected for shrinkage) over the depth on the microdrive scale indicates the discrepancy between both measurements. This correction factor has been established in 26 histologically controlled penetrations in this and other studies [2] as 0.92 (S.D. ±O.I6), i.e. the microdrive readings overestimate the real depth by only 8% on the average. In summary, two conclusions are supported by the data. First, there is no predictability of infragranular preferred directions from the correspondent upper layer values. Second, there is at least a group of lower layer cells with preferred directions rather orthogonal to the correspondent parameter in upper layers. This group seems not to be a small minority, and it therefore consists not only of interneurons but it includes efferent principal neurons, too. The results from AI8 arc similar to the corresponding results from AI? [I, 2]. The functional significance of the shift phenomenon is far from being understood, but it suggests a relative functional autonomy of upper and lower layers as discussed already [2] for the striate area. I Bauer, R., A high probability of an orientation shift between layers 4 and 5 in central parts of the cat striate cortex, Exp. Brain Res., 48 (1982) 245-255. 2 Bauer, R., Differences in orientation and receptive field position between supra- and infragranular cells of cat striate cortex and their possible functional implications, BioI. Cybern., 49 (1983) 137-148. 3 Bauer, R., Dow, B.M. and Vautin, R.O., Laminar distribution of preferred orientations in foveal striate cortex of the monkey, Exp. Brain Res., 41 (1980) 54-60. 4 Bauer, R., Dow, B.M., Snyder, A.Z. and Vautin, R.O., Orientation shift between upper and lower layers in monkey visual cortex, Exp. Brain Res., 50 (1983) 133-145. 5 Hammond, P., Directional tuning of complex cells in area 17 of the feline visual cortex, J. Physiol. (Lond.), 285 (1978) 479-491. 6 Hoffmann, K.-P., Bauer, R., Huber, H.P. and Mayr, 1\1., Single cell activity in area 18 of the eat's visual cortex during optokinetic nystagmus, Exp. Brain Res., 57 (1984) 118-127. 7 Hubel, D.H. and Wiesel, T.N., Receptive fields, binocular interaction, and functional architecture in the eat's visual cortexv J,' Physiol. (Lond.), 160 (1962) 106-157. 8 Hubel, D.H. and Wiesel, T.N., Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. 9 Krueger, J. and Bach, M., Independent systems of orientation columns in upper and lower layers of monkey visual cortex, Neurosci. Lett., 31 (1982) 225-230. 10 Movshon, J.A., Thomson, 1.0. and Tolhurst, D.J. Spatial and temporal contrast sensitivity of neurons in area 17 and 18 of the cats' visual cortex, J. Physiol. (Lond.), 283 (1978) 101-120. II Orban, O.A., Kennedy, H. and Maes, H., Response to movement of neurons in area 17 and 18 of the cat: velocity sensitivity, J. Neurophysiol., 45 (1981) 1043-1058. 12 Tolhurst, D.J., Dean, A.F. and Thomson, 1.0., Preferred direction of movement as an element in the organization of cat visual cortex, Exp. Brain Res., 44 (1981) 340-342. 13 Tretter, F., Cynader, 1\1. and Singer, W., Cat parastriate cortex: a primary or secondary visual area? J. Neurophysiol., 38 (1975) 1099-1113.