Monocular deprivation in kittens differently affects crossed and uncrossed visual pathways

0042-6989/86 53.00 + 0.00 Copyright Q 1986 Pergamon Journals Ltd

Yision yes. Vol. 26. No. 6. pp. 875-884. 1986 Printed in Great Britain. All rights reserved

MONOCULAR DEPRIVATION IN KITTENS DIFFERENTLY AFFECTS CROSSED AND UNCROSSED VISUAL PATHWAYS S. BISTI and G. lstituto

CARMIGNOTO*

di Neurofisiologia de1 CNR, Via S. Zeno, 51, 56100 Pisa, Italy

(Received I November 1984; in finoi revised form 20 September 1985) Abstract-The effects of monocular deprivation (MD) on the crossed and uncrossed visual projections were studied using both electrophysiological and behavioural criteria. Our results show that Visual Evoked Potentials (VEPs) from the deprived eye (DE) in response to contrast reversing gratings are more reduced in the ipsilateral than in the contralateral cortex. This suggests a different sensitivity of the crossed and uncrossed visual pathways to MD. In the behavioural experiments comparable findings were obtained. Cat

Monocular deprivation

Visual cortex

Spatial frequency

INTRODUCTION

Monocular deprivation (MD) during the early months of life induces a profound rearrangement in the organization of the cat striate cortex, whereby the vast majority of cells becomes responsive only to the stimulation of the normal eye (Wiesel and Hubel, 1963, 1965). This change in the ocular dominance of cortical units is similar in areas 17 of both hemispheres, ipsilateral and contralateral to the deprived eye (DE). However single unit recordings in area 18 (Singer, 1978) have shown a consistent difference in the magnitude of ocular dominance shifts of the two hemicortexes, suggesting that the crossed projections to area 18 are more resistant to MD than the uncrossed projections. Nevertheless these results have not been replicated by other authors (Hirsch and Leventhal, 1983). Since electrophysiological data are limited to the ocular dominance distribution of cortical cells, we attempted to compare the effects of MD on the crossed and uncrossed visual projections using both electrophysiological and behavioural measurements. In the electrophysiological experiments we studied Visual Evoked Potentials (VEPs) recorded in response to contrast reversing gratings for both eyes and in the two hemicortexes, ipsilateral and contralateral to the deprived eye. In the behavioural *On leave from FIDIA Research Terme, Padova, Italy.

Laboratories,

VEPs

Visual behaviour

study we measured the visual field of the normal and the deprived eye. As regards the latter, behavioural results reported in the literature are conflicting. Some authors (Van Hof-van Duin, 1977; Heitlaender and Hoffmann, 1978; Hoffmann et al., 1978) showed that in MD cats the visual field of the deprived eye may extend throughout the temporal hemifield, including both monocular and binocular segments. This supports, once again, that the crossed projections, from the nasal retina to the contralateral hemicortex, are less affected by MD than the uncrossed projections, from the temporal retina to the ipsilateral hemicortex. However these results are at variance with those obtained by other authors (Sherman, 1973,1974; Tumosa et al., 1980, 1982; Tieman et al., 1983b), who reported that in MD cats, the orienting responses of the deprived eye are maintained only for the monocular segment of the visual field. We here report that VEPs recorded in monocularly deprived cats show a dramatic difference between the two hemispheres: VEP amplitude in response to stimulation of the DE is much more reduced with respect to the normal eye in the ipsilateral than in the contralateral hemicortex. In the behavioural experiments comparable findings were obtained. MATERIALS

AND METHODS

Experiments were performed in 17 kittens: 6 kittens were used for the behavioural experiments, and 11 for the electrophysiological ones

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Table I. Visual acuity (c/deg) and 2nd harmonic amplitude (JIV) of VEPs recorded in response to the stimulation eye (DE) in the hemisphere ipsilateral (ipsi) and contralateral (contra) to the DE. Kittens were monocularly No. 12’ and No. 15+ were deprived at 18th day

s!

m

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deprivation

in kittens

(see Table 1). Under halothane anaesthesia we sutured the lids of 1 eye of 15 animals at the 35th day, and in 2 kittens at the 18th day after birth. All animals were then reared in the animal quarters to the 4th month of age, at which time the deprived eye was opened. Cortical recordings in 11 animals were made on the day the deprived eye was reopened. Prior to a recording session, anaesthesia was induced with Althesin (1.5 ml/kg), an endotracheal tube and a venous cannula were inserted, and a small piece of skull and dura overlying cortical areas 17 were removed at the corresponding stereotaxic positions of the area centralis. The cat was then immobilized with Pavulon (injected intravenously) and artificially ventilated. PCO, (3.8-4.2%), EEG, body temperature, and heart rate were continuously monitored; anaesthesia was maintained with a continuous infusion of Althesin (0.30 ml/kg/hr). After dilating the pupils with atropine sulphate, optically neutral contact lenses with 3 mm pupils were applied to both eyes and refraction corrected with additional lenses if necessary. At the beginning of the experiment the positions of the papillae and of the area centralis were determined using the technique described by Fernald and Chase (1971). A micropipette filled with NaCl 3 M was inserted into area 17 at the 17-18 border either contralaterally or ipsilaterally to the DE. As soon as the activity of a single unit was well isolated the receptive field was mapped on a tangent screen. In all experiments receptive fields were within 5” of the area centralis. A display oscilloscope, subtending at the cat’s eye 22O*25’ at a distance of 57 cm was centered on the mapped receptive field. The oscilloscope was carefully positioned to cover part of the binocular field including the area centralis of both eyes. Equivalent portions of the upper and the lower visual field were stimulated. VEPs were recorded through the same micropipette. The signal was filtered with bandpass filter (slope 12 dB per octave) between 1 and 60 Hz. Stimulus: sinusoidal gratings of various spatial frequencies and contrast were generated by a computer on the face of a display oscilloscope. The mean luminance was lOcd/m*. Contrast was defined as c = (&I,, -

4nin~K4na.x

+

&in)

where L,,, and L,i, are the maximum and the minimum luminance respectively. A stationary grating was reversed in contrast at 6 Hz (12 rev

affects visual pathways

877

set-I). VEPs recorded, in response to such a stimulus have an approximately sinusoidal waveform [Campbell and Maffei, 1970; see also Fig. I (A-B)] with a temporal frequency of 12 Hz. corresponding to the second harmonic of the stimulus frequency. The signal was averaged on line by a digital PDPI l/O3 computer over 100 stimulus periods in order to improve the signal-to-noise ratio. The averaged noise (100 periods) was usually of the order of 0.1-0.5 pV; the noise was defined as the amplitude of the 12 Hz component of a record obtained in the absence of a contrast stimulus (sampling temporal frequency: 6 Hz). Each spatial frequency and the noise were randomly sampled (3-8 times) during the recording session and the averaged responses at any given spatial frequency were pooled off-line (300-800 stimulus periods), Fourier analyzed and plotted on a X-Y plotter. The amplitude of the 2nd harmonic was used to evaluate the response. As a measure of visual acuity we took the highest spatial frequency at which a potential of 1 PV of amplitude in response to a square wave grating of maximum contrast was recorded. By recording VEPs through a micropipette instead of surface electrodes, it was possible to discriminate between the activity of the two hemispheres. Nevertheless, the field potential recorded through the micropipette (impedance l-2 MR) was well beyond the extension of a hypercolumn, because VEP responses were insensitive to the orientation of the stimulus gratings. Moreover records taken at different cortical depth gave the same results through a range of 3 mm. On the basis of all this evidence we suspect that signals arising from both areas 17 and 18 contribute to the generation of VEP responses. Behaviourai procedures: six kittens were monocularly deprived at the 35th day of age. After 3 months they were tested for their ability to orient to targets in the visual field. Behavioural sessions were performed every day starting from the 4th day after reopening the DE. We followed the same procedure already described in detail by other authors (Sprague and Meikle, 1965; Sherman, 1973, 1974). In short, animals were held by one investigator and were trained to fixate on a target (a piece of food on a wire plus an acoustic clue) presented straight ahead by a second investigator at a distance of 40cm. A novel stimulus (a piece of food on another long wire) was introduced at a distance of 20 cm along one of the guidelines which were

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CARMIGNOTO

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Fig. 1. (A, B) Examples of visual evoked potentials (VEPs) from one kitten (No. 19) monocularly deprived at 35th day after birth and recorded after 3 months of monocular deprivation. The records were obtained from the normal (NE) and the deprived (DE) eye both in &&lateral (A) and contralateral (B) hemisphere. Each record is the average of 600 responses. The spatial frequency is indicated next to each record. (C, D) The second harmonic amplitude of VEPs is plotted as a function of the spatial frequency. Open symbols represent VEP responses to the stimulation of the normal eye (NE), solid symbols represent VEP responses to the stimulation of the deprived eye (DE). The arrows indicate the visual acuity of the two eyes obtained with square gratings of maximum contrast. Stimulus: vertical sinusoidal grating reversed in contrast 12 times/set (6 Hz); contrast, 0.15; mean luminance lOcd/m*. Noise level 0.4 pV.

placed every 15 deg to the left and right to the zero degree fixation line. A positive response was scored if the animals immediately turned their eyes and head towards the novel stimulus. Negative responses were scored in al1 the other cases. Complete determination of the visual field required several days of testing. At the end of the trials about 30 responses for each position were collected. As a control each animal was given a number of blank trials during which the cat was released and the novel stimulus either was not introduced or was introduced outside the visual field. If the cat immediately came to the fixation stimulus this was scored as a negative blank trial. Any other behaviour was scored as a positive response. Every behavioural session was video-recorded for further analysis. RESULTS

V&uaf evoked p~ign~~~l~

We studied the effect of monocular

depri-

vation on the hemisphere ipsilateral or contralateral to the deprived eye by recording visual evoked potentials through a micropipette which allowed us to differentiate the activity of the two hemispheres. Results obtained in one kitten (No. 19) monocularly deprived at the 35th day of age are reported in Figs 1 and 2. Figure l(A, B) shows VEPs recorded in both hemispheres in response to the stimulation of the normal and deprived eye at three spatial frequencies and fixed contrast of the gratings. In the ipsilateral cortex, VEP responses from the DE are smaller than the responses from the normal eye at all spatial frequencies examined. In contrast, in the contralateral cortex, stimulation of both eyes elicits VEPs of comparable amplitude, at least at high spatial frequencies. In Fig. l(C, D) the 2nd harmonic amplitude of the response is reported as a function of the spatial frequency of the stimulus for both eyes. Data points are interpolated with a curve fitted by eye (Campbell and Maffei, 1970; Campbell et at., 1973). On the side ipsilateral to the DE

879

Monocular deprivation in kittens affects visual pathways CONTRALATERAL

IPSILATERAL

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Fig. 2. Second harmonic amplitude (linear scale) of VEPs recorded both ipsilaterally (A-C) and contralaterally (D-F) to the DE plotted as a function of stimulus contrast (logarithmic scale) for three different spatial frequencies: 0.35, 0.7 and 1.4 c/deg. The arrows indicate the contrast threshold obtained, at each frequency, with the extrapolation of the regression line between VEP amplitude and logarithm of contrast to zero voltage level. The regression line have been calculated by the least squares method. The value of noise measured as described in the Methods is indicated by an arrow on the ordinate axis. Symbols and stimulus condition as in Fig. I. Same kitten (No. 19) of Fig. 1.

[Fig. l(C)] the reduction of VEP responses is noticeable at all spatial frequencies and it is particularly evident in the low spatial frequency range. In contrast, contralateral to the DE [Fig. l(D)], VEP responses from the two eyes are very similar, at least at medium and high spatial frequencies, and the values of the acuity are comparable (see also Table 1 and Fig. 3). Figure 2 illustrates for the same cat (No. 19) VEP amplitude as a function of the contrast of the grating at three spatial frequencies. The straight lines were fitted by the least-squares method; points in the saturation range were not included. In the ipsilateral cortex [Fig. 2(A-C)] the contrast threshold (Campbell and Maffei, 1970; Campbell et al., 1973) obtained by extra-

polation of the regression line between evoked potential amplitude and logarithm of contrast to zero voltage level, shows a marked increase for the DE at all spatial frequencies tested. In the contralateral cortex [Fig. 2(D)] VEP responses are very similar and contrast thresholds at all spatial frequencies are practically the same. Noteworthy is that at low spatial frequencies NE and DE present responses of comparable amplitude only for low values of the stimulus contrast. Indeed, at increasing values of contrast, the amplitude of the response from the DE remains practically constant whereas that from the normal eye continues to increase and saturates only at higher levels of the stimulus contrast. This phenomenon was observed

880

S. BISTIand G. CARMICNOTO CONTRALATERAL

IPSILATERAL

Spotiol

frequency

(c/deg

I

Fig. 3. Relative VEP amplitude plotted as a function of spatial frequency for NE and DE. (A, B) Kitten No. 16; contrast 0.17. (C, D) Kitten No. 18; contrast 0.2. (E, F) Kitten No. 20; contrast 0.17. (G, H) Kitten No. 21; contrast 0.17. All kittens were monocularly deprived at 35th day after birth. Symbols and stimulus conditions as in Fig. I.

in all tested kittens with the exception of one (No. 20). Results from 11 kittens are summarized in Table 1. The amplitude in PV of the 2nd harmonic is reported for four spatial frequencies together with the values of visual acuity determined as described in the Methods. Apart from a certain degree of variability among the animals, VEP responses from the DE were always more impaired in the ipsilateral than in the contralateral cortex. The difference is particularly evident if one compares the values of visual acuity for the normal and deprived eye determined in the two hemicortexes. Fig. 3 shows the complete set of data obtained in 4 kittens from our sample. Values are normalized to facilitate the comparison. Recordings obtained from the 2 kittens monocularly deprived at the 18th day of age are shown in Fig. 4. Although there is a ten-

dency (particularly in kitten No. 15) for the deprived eye to exhibit a lower visual acuity than the normal eye in the hemisphere contralateral to the DE, even in these animals, in which the effect of MD is stronger, the reduction in VEP responses is more pronounced in the ipsilateral than in the contralateral cortex. Thus these results are very similar to those obtained in kittens deprived at the 35th day (Figs l-3; Table 1). Behaviourai results The eiectrophysiological results suggested that the less pronounced effect of MD on the crossed visual pathway might be reflected in less impairment of DE vision in the temporal hemifield, since it is subserved by the crossed retino-geniculo-cortical projections. Therefore the cats were tested for their ability to orient to targets at different positions in the visual space.

881

Monocular deprivation in kittens affects visual pathways CONTRALATERAL

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Fig. 4. Relative VEP amplitude plotted as a function of spatial frequency for NE and DE in two kittens monocularly deprived at 18th day after birth. (A, B) Kitten No. 12; contrast 0.15. (C, D) Kitten No. 15; contrast 0.17. Symbols and stimulus conditions as in Fig. 1.

In particular, kittens were first trained to orient to targets using their experienced eye and this was in all respects normal. When kittens were tested using their deprived eye (starting at the 4th day after reopening) their behaviour was highly abnormal. At the beginning all the animals ignored stimuli presented in the binocular part of the visual field and they oriented only toward stimuli presented in the monocular segment. After 4 or 5 days of testing some orienting responses appeared at 30 and 15” in the temporal visual field and the percentage of positive trials increased over time but it never reached a normal value. Data obtained in three subsequent sessions after 2 weeks of training of 6 MD kittens and 1 normal adult cat were pooled together and reported in Fig. 5. The percentage of positive responses at different positions in the visual field is reported as polar plot. In agreement with previous investigators (van Hof-van Duin, 1977; Heitlaender and Hoffmann, 1978; Hoffmann et al., 1978) we found that, after monocular deprivation, visual orienting responses are not limited to the monocular segment of the visual field, but extend to the binocular portion of the temporal hemifield. This contrasts with results obtained by other authors (Sherman 1973, 1974; Tumosa

et al., 1980, 1982; Tieman et al., 1983b) and this discrepancy does not seem to be due to experimental conditions, since all the investigators followed exactly the same procedures. It is noteworthy that in our case, kittens were allowed a period of normal binocular vision before eye occlusion, whereas all the other authors performed the eyelid suturing at the time of the natural eye opening.

wscussloN

Dl$erent susceptibility of crossed and uncrossed visual pathways to MD We have reported that in monocularly deprived cats VEP responses from the deprived eye are more reduced with respect to the normal eye when recorded from the ipsilateral than from the contralateral visual cortex. These results are apparently in good agreement with those obtained ~ha~ourally in the MD kittens. In fact some orienting responses are maintained in the binocular part of the temporal hemifield (Fig. 5). A stronger impairment of the uncrossed with respect to the crossed visual pathway, was already observed following unequal alternating monocular exposure (Tumosa et al., 1980, 1982; Tieman et al., 1983a, b; Tieman et al., 1984).

S. BISTIand G. CARMIGNOTO

882

RIGHT

RIGHT

EYE (NE)

EYE

0

50

100 VISUAL

0 PERFORMANCE

50

100

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Fig. 5. Visual field perimetry for the right eye of six kittens monocularly deprived at 35th day of age and tested after 3 months of MD and one normal adult cat. The visual field is represented by polar plot in which segments along the guidelines show the mean value of positive responses expressed in percent. The percentage of blank positive trials is indicated on the zero position of the plot.

The profound deficit of the ipsilateral visual pathway, which corresponds to the loss of the nasal hemifield, could be the neural correlate in the cat of the phenomenon of the “fixed monocular amblyopia” in man (Jampolsky, 1978). In fact in both esotropes and exotropes subjects with very severe amblyopia, vision in the nasal hemifield is much more impaired than in the temporal one, and in some cases it is totally suppressed. One possible explanation for the fact that the uncrossed visual pathway is more sensitive to MD could be related to the immaturity of this pathway at the time of lid closure. Indeed, Sireteanu and Maurer (1982) reported that the development of the kitten’s visual field is still

ongoing postnatally and claimed that until 7-8 weeks performance was significantly poorer in the nasal than in the temporal field. Similar results were obtained in psychophysical experiments in human infants (Lewis et al., 1979). Therefore, since according to these behavioural results the uncrossed projections are still in a developing stage the sensory deprivation starting at 3-5 weeks of age might mainly affect these projections. Anatomical data showing a later development of the uncrossed projections have been obtained either in postnatal studies in hamsters (So et al., 1978) or prenatally in kittens (Shatz, 1983). Furthermore, an indirect evidence that this immaturity could be present postnatally in kittens has been reported by

Monocular

deprivation

in kittens affects visual pathways

Silverman (1982). He reported utilizing 14C-2deoxyglucose autoradiographic technique that the ocular dominance columns develop first and are more apparent during the first month of life in the hemisphere contralateral to the stimulated eye. An alternative hypothesis is that the greater susceptibility might be related to the cellular populations in the two hemiretinae, which have been shown to be different either in distribution or in phylogenetical history (Stone et al., 1980). These authors suspected that the main difference between temporal and nasal retina is due to a higher proportion of medium size ganglion cells in the temporal retina. The same difference in cellular composition could be maintained at higher levels i.e. crossed vs uncrossed retino-geniculo-cortical projections, and thus this could provide an anatomical basis for the electrophysiological and behavioural data. Finally it should be also taken into account that the crossed projection is composed of a larger number of fibres compared to the uncrossed projection. According to Stone (1966) 25% of the ganglion cells in the temporal retina projects contralaterally. These data have been confirmed and extended (see for references Illing and Wlssle, 1981). Moreover the crossed projections appear to be more numerous than the uncrossed projections following their appearance during development (Anker, 1977). It might be that the larger number of fibres in the crossed visual pathway may be related to their higher resistance to the effect of MD. Comparison between VEP and single unit results Single unit recordings performed in monocularly deprived cats (Wiesel and Hubel, 1963, 1965; see for review Sherman and Spear, 1982) have shown that the majority of striate neurones became unresponsive to the stimulation of the DE, and that the percentage of neurones still responding to the DE is similar in the two hemispheres. While the reduction of VEP amplitude at all spatial frequencies in the hemisphere ipsilateral to the DE could be explained in terms of the reduced number of responsive neurones, this cannot explain the presence of VEPs of approximately normal amplitude in the contralateral hemisphere. Therefore a different hypothesis for the VEP results has to be considered. In normal adult animals VEPs are probably generated by the slow wave components (EPSP and IPSP) related to both cortical inputs and

883

intracortical activities (see for reference Petshe et al., 1984). In MD cats there are practically no cortical neurones responding to the DE. It might be that in this condition VEP responses from the DE are mainly generated by the geniculo-cortical input. If so the asymmetrical reduction of VEPs reflects an asymmetrical impairment of the crossed and uncrossed visual inputs. Indeed, in the cortex contralateral to the DE where VEPs of approximately normal amplitude at medium and high spatial frequencies were recorded, the visual input seems to be present but somehow unable to appropriately drive the response of single cortical neurones. The large reduction of VEP responses at low spatial frequencies which is present also in the contralateral hemisphere and already reported by other authors (Snyder and Shapley, 1979; Bonds et al., 1980; Freeman et al., 1983), suggest that fibres carrying low frequency information, supposedly the Y-system (see for review Sherman and Spear, 1982), are more susceptible to deprivation. An additional pertinent observation with regard to our results is that in MD cats the visual acuity for the DE, when determined behaviourally (Mitchell et al., 1976, 1977; Smith, 1981), is reduced with respect to the NE. Interestingly, it has values of the same order as those obtained with VEPs in the ipsilateral cortex reported in the present study (Table 1). In this context, after enucleation of the normal eye an improvement of the DE visual acuity has been reported (Smith, 1981). This could be due to a withdrawal of an active inhibition from the normal eye. The fact that VEPs recorded in the contralateral hemisphere showed the presence of a relevant input could offer the physiological basis for the above-mentioned behavioural result (Smith, 1981). In conclusion our results show that the effect of monocular deprivation on visual pathways is asymmetrical, in that, the uncrossed projections from the temporal retina to the ipsilateral cortex is much more impaired than the crossed projections from the nasal retina to the contralateral cortex. This result could account for the maintenance of some visual orienting responses in the binocular portion of the temporal hemifield of MD kittens. Acknowledgements-We Fiorentini, and critical

thank

A. Leon and L. Maffei reading

Tacchi,

M. Antoni

and M.

Benvenuti

Drs

of the manuscript; and P. Taccini

L.

Chalupa,

A.

for helpful discussions we also thank

for technical

for typing the manuscript.

A.

assistance

884

S. BISTIand G. CARMIGHOTO

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