8 1991 Gordon and
Intern. J . Neuroscience, 1991, Vol. 58, pp. 255-259 Reprints available directly from the publisher Photocopying permitted by license only
Breach, Science Publishers S.A Printed in the United Kingdom
Brief Communication CONTRAST RESPONSES TO BRIGHT SLITS OF VISUAL CELLS IN THE SUPERIOR COLLICULUS OF THE ALBINO RAT F. GONZALEZ", R. PEREZ", C. ACURA", J. M. ALONSO" and J. L. LABANDEIRA-GARCIA'
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
Departamento de Fisiologia" and Departamento de Ciencias Morfologicas', Faculiad de Medicina, Santiago de Compostela, Spain (Received December 15, 1990) Contrast is the most effective stimulus in the visual system. The response of single cells to changes in stimulus contrast has been studied in a large variety of animals and the contrast response function determined. In the rat, studies on responses to contrast have been focused primarily in the geniculocortical pathway and there are relatively few in subcortical structures. We report here for the first time the contrast response function of single units located in the superior colliculus (SC) of the albino rat to several stimulus contrast. Cells in the SC require a relatively high contrast to elicit a reliable response and the dynamic response range is restricted to a short contrast interval. Keywords: albino rat. contrast. superior colliculus
The effect of contrast on the responses of visual cells has been studied in a variety of mammals. In the rat some studies have been undertaken in order to determine the contrast response characteristics of visual cells (Powers & Green, 1978; Lennie & Perry, 1981; Harnois et al., 1984; Silveira et al., 1987) and the effect of bright and dark adaptation to the receptive field (RF) organization of retinal ganglion cells (Cicerone & Green, 1980a, b). In the rat, these studies on contrast sensitivity have been focused primarily on the geniculocortical visual pathway while other relevant subcortical visual structures have been rather neglected. The superior colliculus (SC), although having multisensory roles, is still regarded as a relevant subcortical visual structure (Stein, 1984). In the present report we describe the responses of cells in the SC of the albino rat to bright moving slits with several background luminances and stimulus contrast. MATERIAL AND METHODS The experiments were carried out in adult albino rats (Sprage-Dawley). The animals were initially anesthetized with an intraperitoneal injection of 49 mg/Kg of ketamine (Ketolar, Parke-Davis) and 3.3 mg/Kg of xylacin (Rompun, Bayer), paralyzed with a dose of 13mg/Kg of pancuronium bromide (Pavulon, Organon) and artificially respirated with a mixture of N,O (30%), 0, (70%) and halothane (0-2%). A heating pad ensured the constant temperature of the animal. The ECG was continuously monitored and used as a reference for halothane dose. The animals were placed on
?We are grateful to the Xunta de Galicia and DGICYT for their financial support and to Luz Casas for her technical assistance. J. M. Alonso and R. Perez were fellows of Diputacion Provincial of A Corufia and Xunta de Galicia respectively. 255
256
F. GONZALEZ et a1
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
a stereotaxic frame with a frontal translucent panel on which a galvanometer mirror system projected the visual stimulus. Single cell recordings were made by means of Pt-Ir microelectrodes and electrolytic lesions were made at the end of the most relevant penetrations for further histological reconstruction (Acuiia et al. 1990). A computer controlled the data recording and the stimulus which consisted of a white bright slit sweeping across the cell's RF. The stimulus velocity ranged from 10 to lOO"/s. Slits are small localized stimuli and therefore changes in their luminance practically do not affect the mean luminance of the retina. Changes in contrast can therefore be obtained by modifying the slit luminance. The basic exploration consisted in sweeping the bar across the cell's R F with a background luminance of 0.05 cd/m2 and various stimulus luminances. Luminances were measured with a Sekonic Digi-spot photometer and the contrast of the stimulus was determined using the formula:
c =
Imax Imin
-
Imin
+ Imax
x 100
where Imax is the slit luminance and Imin is the luminance of the panel. Under each stimulus condition, the spikes of the cell were collected for about 50 sweeps, averaged and normalized, where the maximal response for each cell was taken as 100%. RESULTS During the experiments, 60 cells from the SC responding to visual stimulation were studied quantitatively in order to determine the properties of their receptive fields, and qualitatively to test their responses to several stimulus contrasts. A subset of 11 cells, 8 from superficial and 3 from deep layers, which make up the quantitative dataset of this report, were tested in detail for responses to several stimulus contrasts. An increase in cell response along with the stimulus contrast were observed. The qualitative observations made in the remaining 49 single cells and background activity as well, give support to these quantitative data. The size of their receptive fields ranged from 5 to 30" and they were located within the frontal visual field subserving a solid angle of about 90". The cells were classified in OFF or ON-OFF types according to their responses to flashing bars. No cells with only ON responses were found. Of the 1 1 cells 9 showed phasic responses and the remaining 3 cells showed tonic responses. Direction selectivity was evident in 2 cells. The quantitative study of these units demonstrated a clear relationship between stimulus contrast and cell response. Figure 1 shows the normalized responses of four cells expressed as the percentage of the maximal response, plotted against the stimulus contrast under a background luminance of 0.05 cd/m'. The contrast response function (CRF) of these cells demonstrates an increase of cell response as the stimulus contast increased. Under dim background conditions (0.05 cd/m2)the minimum threshold of contrast needed to elicit a reliable cell response is rather high (around 90%). From that threshold on, the slope of the cell response rises steeply. The C R F seems to be similar in upper and lower collicular layers as can be seen for cells RBJ and RBQ in Figure 1, recorded from upper and lower layers respectively. In order to test the effect of background luminance on the cell C R F a contrast series was made with several background luminances. In Figure 2 the C R F of two collicular cells under various background luminances is shown. A variation in the location of the dynamic response range over the contrast axis can be observed in both cells. Under dim background conditions (0.05 cd/m2) the dynamic response range (the
CONTRAST RESPONSES IN RAT SC 0 REV
lOO-
-
257
0 REX RE0 0 RE1
0.05cd/m2
Lu 0
z
0
a E U
50-
x
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
Pn
0-
I
contrast range over which the cell's response increases with contrast) is restricted approximately to the upper 20% of contrast, whereas under higher background luminance conditions it shifts leftwards. Under bright background the contrast threshold to elicit cell responses lowers down to approximately 25% in the first case and to 50% in the second.
DISCUSSION
A relevant finding in our experiments was that collicular cells in the albino rat require a high stimulus contrast to elicit a reliable cell response. That, although not explicitly
A
B
1
a
50
I
100
(%I
FIGURE 2 Contrast response function of two collicular cells (A and B) plotted against stimulus contrast under different background luminances Cell response is represented as in Figure 1. In both cases, A and B. a shift leftwards in the dynamic response range can be seen.
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
258
F. GONZALEZ ei al.
reported, can be also inferred form works done by other authors who use high contrasts in their experiments with rats: in the visual cortex (Harnois et al. 1984; Waterhouse et al. 1990; Shaw et al. 1975), superior colliculus (Humphrey 1968), retinal ganglion cells (Powers & Green, 1978) and lateral geniculate nucleus (Lennie & Perry, 1981). The requirement of high contrast to trigger cell activity may therefore be a common feature in the rat visual system. Responses to changes in background luminance have been described in ganglion cells (Brown & Rojas, 1965) and cortical cells (Wiesenfeld & Kornel, 1975; Shaw et al. 1975) of the rat. In the cells located in the superficial layers of the mouse SC, very little response to diffuse background illumination was reported (Drager & Hubel, 1975). Fukuda and Iwama (1978) described cells (type IVc of their classification) responding only to diffuse light at either ON or OFF and not to a delimited bright spot flashed over their receptive field. In our experiments we did not find responses in coilicular cell activity when the background luminance was turned ON o r OFF. However, background luminance modified the cell C R F in the sense that lower contrasts were needed to elicit responses at higher levels of light adaptation. The SC of the rat receives direct input mainly from retinal ganglion cells and from the visual cortex, particularly the superficial layers (Fukuda & Iwama, 1978). Of 11 cells reported here 8 were located within superficial layers and they may therefore receive direct input from retinal ganglionic cells. According to this, the changes in the CRF of collicular cells may be due to light adaptation processes which take place at retinal level (Cicerone & Green, 1980a, b; Green, 1971). Although for some R F properties the neurons of the rat SC have been proved to differ depending on their locations in depth (Fukuda & Iwama, 1978; Humphrey, 1968) we do not have evidence supporting this with respect to the constrast responses. Our data demonstrate that the cell responses in the albino rat are related to the stimulus contrast and that high contrasts are a requirement of the albino rat collicular cells. The detailed mechanisms responsible for that are, however, difficult to disentangle. REFERENCES Acu~ia,C., Cudeiro, J., Gonzalez, F., Alonso, J. M., & Perez, R. (1990). Lateral-posterior and pulvinar reaching cells. Comparison with parietal area 5a: study in behaving macaca nemestrina monkeys. Experimental Brain Research, 82, 158-166. Brown, J. E. & Rojas, J. A. (1965). Rat retinal ganglion cells: receptive field organization and maintained activity. Journal qf Neurophysiology, 28, 1073-1090. Cicerone, C. M . & Green, D. G. (1980a). Light adaptation within the receptive field center of rat ganglion cells. Journal of Physiology (Lond.), 301, 517-534. Cicerone, C. M. & Green, D. G . (1980b). Dark adaptation within the receptive field center of rat ganglion cells. Journal of Physiology (Lond.), 301, 535-548. DrLger, U. C. & Hubel, D. H. (1975). Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. Journal of Neurophysiology, 38, 690-7 13. Fukuda Y. and lwama K . (1978). Visual receptive-field properties of single cells in the rat superior colliculus. Japanese Journal of Physiology, 28, 385-400. Green, D. S. (1971). Light adaptation in the rat retina: Evidence for two receptor mechanisms. Science, 174, 598-600. Harnois, C., Bodis-Wollner, I., & Onofrj, M. (1984). The effect of contrast and spatial frequency on the visual evoked potential of the hooded rat. Experirnenfal Brain Research, 57, 1-8. Humphrey, N. K. (1968). Responses to visual stimuli of units in the superior colliculus of rates and monkeys. Experirnenlal Neurology, 20, 3 12-340. Lennic, P. & Perry, V. H. (1981). Spatial contrast sensitivity of cells in the lateral geniculate nucleus of the rat. Journal of Physiology (Lond.), 315, 69-79. Powers, M. K . & Green, D. G. (1978). Single retinal ganglion cell responses in the dark-reared rat: grating acuity, contrast sensitivity and defoccusing. Vision Research, 18, 1533-1539.
CONTRAST RESPONSES IN RAT SC
259
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
Shaw, C., Yinon, U., & Auerbach, E. (1975). Receptive fields and response properites of neurons in the rat visual cortex. Visual Research, IS, 203-208. Silveira, L. C. L., Heywood, C. A,, & Cowey, A. (1987). Contrast sensitivity and visual acuity of the pigmented rat determined electrophysiologically. Vision Research, 27, 1719-1731. Stein, B. E., (1984). Development of the superior colliculus. Annual Review of Neuroscience, 7 , 95-125. Waterhouse, B. D., Azizi, S. A., Burne, R. A,, & Woodward, D. J. (1990). Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin rnicroiontophoresis. Bruin Research, 514, 276-292. Wiesenfeld, Z . , & Kornel, E. E. (1975). Receptive fields of single cells in the visual cortex of the hooded rat. Bruin Research, 94, 401-412.
Intern. J . Neuroscience, 1991, Vol. 58, pp. 255-259 Reprints available directly from the publisher Photocopying permitted by license only
Breach, Science Publishers S.A Printed in the United Kingdom
Brief Communication CONTRAST RESPONSES TO BRIGHT SLITS OF VISUAL CELLS IN THE SUPERIOR COLLICULUS OF THE ALBINO RAT F. GONZALEZ", R. PEREZ", C. ACURA", J. M. ALONSO" and J. L. LABANDEIRA-GARCIA'
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
Departamento de Fisiologia" and Departamento de Ciencias Morfologicas', Faculiad de Medicina, Santiago de Compostela, Spain (Received December 15, 1990) Contrast is the most effective stimulus in the visual system. The response of single cells to changes in stimulus contrast has been studied in a large variety of animals and the contrast response function determined. In the rat, studies on responses to contrast have been focused primarily in the geniculocortical pathway and there are relatively few in subcortical structures. We report here for the first time the contrast response function of single units located in the superior colliculus (SC) of the albino rat to several stimulus contrast. Cells in the SC require a relatively high contrast to elicit a reliable response and the dynamic response range is restricted to a short contrast interval. Keywords: albino rat. contrast. superior colliculus
The effect of contrast on the responses of visual cells has been studied in a variety of mammals. In the rat some studies have been undertaken in order to determine the contrast response characteristics of visual cells (Powers & Green, 1978; Lennie & Perry, 1981; Harnois et al., 1984; Silveira et al., 1987) and the effect of bright and dark adaptation to the receptive field (RF) organization of retinal ganglion cells (Cicerone & Green, 1980a, b). In the rat, these studies on contrast sensitivity have been focused primarily on the geniculocortical visual pathway while other relevant subcortical visual structures have been rather neglected. The superior colliculus (SC), although having multisensory roles, is still regarded as a relevant subcortical visual structure (Stein, 1984). In the present report we describe the responses of cells in the SC of the albino rat to bright moving slits with several background luminances and stimulus contrast. MATERIAL AND METHODS The experiments were carried out in adult albino rats (Sprage-Dawley). The animals were initially anesthetized with an intraperitoneal injection of 49 mg/Kg of ketamine (Ketolar, Parke-Davis) and 3.3 mg/Kg of xylacin (Rompun, Bayer), paralyzed with a dose of 13mg/Kg of pancuronium bromide (Pavulon, Organon) and artificially respirated with a mixture of N,O (30%), 0, (70%) and halothane (0-2%). A heating pad ensured the constant temperature of the animal. The ECG was continuously monitored and used as a reference for halothane dose. The animals were placed on
?We are grateful to the Xunta de Galicia and DGICYT for their financial support and to Luz Casas for her technical assistance. J. M. Alonso and R. Perez were fellows of Diputacion Provincial of A Corufia and Xunta de Galicia respectively. 255
256
F. GONZALEZ et a1
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
a stereotaxic frame with a frontal translucent panel on which a galvanometer mirror system projected the visual stimulus. Single cell recordings were made by means of Pt-Ir microelectrodes and electrolytic lesions were made at the end of the most relevant penetrations for further histological reconstruction (Acuiia et al. 1990). A computer controlled the data recording and the stimulus which consisted of a white bright slit sweeping across the cell's RF. The stimulus velocity ranged from 10 to lOO"/s. Slits are small localized stimuli and therefore changes in their luminance practically do not affect the mean luminance of the retina. Changes in contrast can therefore be obtained by modifying the slit luminance. The basic exploration consisted in sweeping the bar across the cell's R F with a background luminance of 0.05 cd/m2 and various stimulus luminances. Luminances were measured with a Sekonic Digi-spot photometer and the contrast of the stimulus was determined using the formula:
c =
Imax Imin
-
Imin
+ Imax
x 100
where Imax is the slit luminance and Imin is the luminance of the panel. Under each stimulus condition, the spikes of the cell were collected for about 50 sweeps, averaged and normalized, where the maximal response for each cell was taken as 100%. RESULTS During the experiments, 60 cells from the SC responding to visual stimulation were studied quantitatively in order to determine the properties of their receptive fields, and qualitatively to test their responses to several stimulus contrasts. A subset of 11 cells, 8 from superficial and 3 from deep layers, which make up the quantitative dataset of this report, were tested in detail for responses to several stimulus contrasts. An increase in cell response along with the stimulus contrast were observed. The qualitative observations made in the remaining 49 single cells and background activity as well, give support to these quantitative data. The size of their receptive fields ranged from 5 to 30" and they were located within the frontal visual field subserving a solid angle of about 90". The cells were classified in OFF or ON-OFF types according to their responses to flashing bars. No cells with only ON responses were found. Of the 1 1 cells 9 showed phasic responses and the remaining 3 cells showed tonic responses. Direction selectivity was evident in 2 cells. The quantitative study of these units demonstrated a clear relationship between stimulus contrast and cell response. Figure 1 shows the normalized responses of four cells expressed as the percentage of the maximal response, plotted against the stimulus contrast under a background luminance of 0.05 cd/m'. The contrast response function (CRF) of these cells demonstrates an increase of cell response as the stimulus contast increased. Under dim background conditions (0.05 cd/m2)the minimum threshold of contrast needed to elicit a reliable cell response is rather high (around 90%). From that threshold on, the slope of the cell response rises steeply. The C R F seems to be similar in upper and lower collicular layers as can be seen for cells RBJ and RBQ in Figure 1, recorded from upper and lower layers respectively. In order to test the effect of background luminance on the cell C R F a contrast series was made with several background luminances. In Figure 2 the C R F of two collicular cells under various background luminances is shown. A variation in the location of the dynamic response range over the contrast axis can be observed in both cells. Under dim background conditions (0.05 cd/m2) the dynamic response range (the
CONTRAST RESPONSES IN RAT SC 0 REV
lOO-
-
257
0 REX RE0 0 RE1
0.05cd/m2
Lu 0
z
0
a E U
50-
x
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
Pn
0-
I
contrast range over which the cell's response increases with contrast) is restricted approximately to the upper 20% of contrast, whereas under higher background luminance conditions it shifts leftwards. Under bright background the contrast threshold to elicit cell responses lowers down to approximately 25% in the first case and to 50% in the second.
DISCUSSION
A relevant finding in our experiments was that collicular cells in the albino rat require a high stimulus contrast to elicit a reliable cell response. That, although not explicitly
A
B
1
a
50
I
100
(%I
FIGURE 2 Contrast response function of two collicular cells (A and B) plotted against stimulus contrast under different background luminances Cell response is represented as in Figure 1. In both cases, A and B. a shift leftwards in the dynamic response range can be seen.
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
258
F. GONZALEZ ei al.
reported, can be also inferred form works done by other authors who use high contrasts in their experiments with rats: in the visual cortex (Harnois et al. 1984; Waterhouse et al. 1990; Shaw et al. 1975), superior colliculus (Humphrey 1968), retinal ganglion cells (Powers & Green, 1978) and lateral geniculate nucleus (Lennie & Perry, 1981). The requirement of high contrast to trigger cell activity may therefore be a common feature in the rat visual system. Responses to changes in background luminance have been described in ganglion cells (Brown & Rojas, 1965) and cortical cells (Wiesenfeld & Kornel, 1975; Shaw et al. 1975) of the rat. In the cells located in the superficial layers of the mouse SC, very little response to diffuse background illumination was reported (Drager & Hubel, 1975). Fukuda and Iwama (1978) described cells (type IVc of their classification) responding only to diffuse light at either ON or OFF and not to a delimited bright spot flashed over their receptive field. In our experiments we did not find responses in coilicular cell activity when the background luminance was turned ON o r OFF. However, background luminance modified the cell C R F in the sense that lower contrasts were needed to elicit responses at higher levels of light adaptation. The SC of the rat receives direct input mainly from retinal ganglion cells and from the visual cortex, particularly the superficial layers (Fukuda & Iwama, 1978). Of 11 cells reported here 8 were located within superficial layers and they may therefore receive direct input from retinal ganglionic cells. According to this, the changes in the CRF of collicular cells may be due to light adaptation processes which take place at retinal level (Cicerone & Green, 1980a, b; Green, 1971). Although for some R F properties the neurons of the rat SC have been proved to differ depending on their locations in depth (Fukuda & Iwama, 1978; Humphrey, 1968) we do not have evidence supporting this with respect to the constrast responses. Our data demonstrate that the cell responses in the albino rat are related to the stimulus contrast and that high contrasts are a requirement of the albino rat collicular cells. The detailed mechanisms responsible for that are, however, difficult to disentangle. REFERENCES Acu~ia,C., Cudeiro, J., Gonzalez, F., Alonso, J. M., & Perez, R. (1990). Lateral-posterior and pulvinar reaching cells. Comparison with parietal area 5a: study in behaving macaca nemestrina monkeys. Experimental Brain Research, 82, 158-166. Brown, J. E. & Rojas, J. A. (1965). Rat retinal ganglion cells: receptive field organization and maintained activity. Journal qf Neurophysiology, 28, 1073-1090. Cicerone, C. M . & Green, D. G. (1980a). Light adaptation within the receptive field center of rat ganglion cells. Journal of Physiology (Lond.), 301, 517-534. Cicerone, C. M. & Green, D. G . (1980b). Dark adaptation within the receptive field center of rat ganglion cells. Journal of Physiology (Lond.), 301, 535-548. DrLger, U. C. & Hubel, D. H. (1975). Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. Journal of Neurophysiology, 38, 690-7 13. Fukuda Y. and lwama K . (1978). Visual receptive-field properties of single cells in the rat superior colliculus. Japanese Journal of Physiology, 28, 385-400. Green, D. S. (1971). Light adaptation in the rat retina: Evidence for two receptor mechanisms. Science, 174, 598-600. Harnois, C., Bodis-Wollner, I., & Onofrj, M. (1984). The effect of contrast and spatial frequency on the visual evoked potential of the hooded rat. Experirnenfal Brain Research, 57, 1-8. Humphrey, N. K. (1968). Responses to visual stimuli of units in the superior colliculus of rates and monkeys. Experirnenlal Neurology, 20, 3 12-340. Lennic, P. & Perry, V. H. (1981). Spatial contrast sensitivity of cells in the lateral geniculate nucleus of the rat. Journal of Physiology (Lond.), 315, 69-79. Powers, M. K . & Green, D. G. (1978). Single retinal ganglion cell responses in the dark-reared rat: grating acuity, contrast sensitivity and defoccusing. Vision Research, 18, 1533-1539.
CONTRAST RESPONSES IN RAT SC
259
Int J Neurosci Downloaded from informahealthcare.com by UB Giessen on 12/14/14 For personal use only.
Shaw, C., Yinon, U., & Auerbach, E. (1975). Receptive fields and response properites of neurons in the rat visual cortex. Visual Research, IS, 203-208. Silveira, L. C. L., Heywood, C. A,, & Cowey, A. (1987). Contrast sensitivity and visual acuity of the pigmented rat determined electrophysiologically. Vision Research, 27, 1719-1731. Stein, B. E., (1984). Development of the superior colliculus. Annual Review of Neuroscience, 7 , 95-125. Waterhouse, B. D., Azizi, S. A., Burne, R. A,, & Woodward, D. J. (1990). Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin rnicroiontophoresis. Bruin Research, 514, 276-292. Wiesenfeld, Z . , & Kornel, E. E. (1975). Receptive fields of single cells in the visual cortex of the hooded rat. Bruin Research, 94, 401-412.
