Child: care, health and development. 1979. 5. 375-383
PHYSIOLOGICAL BASIS OF VISUAL ACUITY AND ITS DEVELOPMENT IN KITTENS
H. IKEDA The Rayne Institute, St Thomas's Hospital, London Accepted for publication 16 July 1979
Summary To answer the questions, (1) Which cells in the visual system arc responsible for high visual acuity and (2) Does the function of the cells which provide high visual acuity develop postnatally; single cell studies have been made in the retina, lateral geniculate nucleus (LGN) and visual cortex of cats of different ages. Sustained-X retinal ganglion cells in the area centralis (the equivalent retinal position to the human fovea) set the upper limit of visual acuity. The cellular acuity develops postnatally until it reaches the adult level at 3-4 months-of-age. The improvement of acuity is associated with an increase in the strength of the inhibitory surround mechanism of the receptive field of sustained cells in the area centralis. The maturation of cellular acuity coincides with maturation ol retinal and LGN synaptic organisation and of optic nerve myelination. Visual acuity is an important function of the fovea, the part of the retina which receives the image of an object on which the eye fixates. It is a measure of the minimum detectable angle between two points. Two questions have been asked regarding the physiological basis of visual acuity, using the cat as an animal model. The cat fixates with the area centralis, the area free from blood vessels in the retina where the density of cones and retinal ganglion cells is highest, as in man (Bishop et al. 1962, Steinberg et al. 1973, Stone 1965, Hughes 1974). The two questions are: (1) Which cells in the visual system are responsible for providing the physiological basis for high visual acuity in the mature visual system? (2) Does the function of the cells which provide high visual acuity develop postnatally? I Which cells in the li.sual .system provide rhe physiological basis for high visual acuity? Although without properly functioning cones there can be no high visual 0305-1862/79/1200-037552.00
© 1979 Blackwell Scientific Publications
375
376
H. Ikcda
acuity, visual acuity is the minimum detectable angle between points on a contrasting background and ihus involves the detection of fine contrast. The first cells in the visual system which show such a function clearly are the retitial ganglion cells (Kuffler 1953). We need neurons which respond to stimuli brighter than background in order to see a while letter on a grey background, which are on-centre cells in neurophysiological classification. We also need neurons which respond to stimuli darker than background, which are off-centre cells in neurophysiological classification, in order to see a black letter on a white background. Indeed the on-centre and ofT-centre retinal ganglion cells may provide the physiological basis for contrast detection necessary for visual acuity. But is a specific cell type needed, whether on-cenire or otT-centre. in order to see a very small object, thus achieving high visual acuity? The answer appears to be 'yes'. Neurophysiological studies of retinal ganglion cells and cells in the afferent visual pathway have suggested parallel processing of two aspects of visual information, i.e. spatial discrimination and rapid movement detection, which are initiated from two major types of retinal ganglion cells, regardless of whether the cell is on-centre or ofT-centre (EnrothCugell&Robson !966.Fukada l97I.CleIande/fl/. 1971, Ikeda& Wright 1972). The two types are 'sustained" or 'X' cells and 'transient" or 'Y' cells. As the names suggest, sustained cells are those cells which respond with sustained firing to a stationary stimulus as long as the stimulus is within the receptive field of the cell, while transient cells are those which give only transient firing when the stimulus is presented, but ignore the stimulus soon afterwards. As Figure I illustrates, sustained cells have been identified as beta cells morphologically and have a small cell body and small dendritic field, while transient cells are alpha cells and have a large cell body and large dendritic field (Boycott & Wassle 1974). Sustained cells have very small receptive fields and strong inhibitory surrounds which is the property of linear spatial summation and many other characteristics which are suitable for spatial analysis, while transient cells have properties which are suitable for detection of rapid and coarse movement and initiation of the fixation reflex (Ikeda & Wright 1972). These findings led to the suggestion that it is the 'sustained-X' cell that provides the physiological basis for high visual acuity. This suggestion has been confirmed by experiments in which the visual acuity of individual cells was measured using slowly moving sinusoidal gratings of different line widths, starting from very coarse gratings and gradually challenging the cell with progressively finer gratings. The visual acuity of
Development of visual acuity in kittens
377
Which cell? ANATOMICAL CLASS
PHYSIOLOGICAL CLASS
Alpha cell
(by response to steady stimulus} Transient- Y (Stimulus size I
2.0=
FUNCTIONAL ROLE
Deteclion of rapid movement Initiation of fixation reflex
spikes/sec SuslQined-x Beta cell
[
(Stimulus size • 0.
oi-
Spatial discriminotlon Visual acuity Contrast sensitivity
20 sec.
StimulusJ
On
n
Off
F I G U R E 1. Two major physiological lypes of retinal ganglion cells (transient-Y and suslained-X) correlated with the morphological classificalion of BoycoU and Wiissle (1974) atid their tiring patiern lo an optimal stimulus spot at the receptive field centre. The size of the optimal stimulus, i.e. the stimulus which produces the best response from the cell, is different for transient and sustained cells. Visualacuity is produced by sustained-X cells, morphologically the beta cell
a ceil can be defined as the finest grating to which the cell responds by firing to the individual lines: in other words "recognising* the lines. Measurements of cellular visual acuity have been made in retinal ganglion cells, in cells of layers A and Al ofthe lateral geniculate nucleus (LGN) and in cells of area 17 ofthe visual cortex in normal adult cats, under general anaesthesia. The method and the conditions of measurement have been described in detail elsewhere (Ikcda & Wright 1976). In Figure 2 the visual acuity of sustained retinal ganglion cells (a), transient retinal ganglion cells (b), sustained LGN cells (c) and transient LGN cells (d) is expressed in terms ofthe spatial frequency of a grating, i.e. thenumberof black and white lines in 1 degree of visual angle, which can be resolved by cells, plotted against the retitial eccentricity. The crosses in Figure 2 c and d were obtained from cells in the visual cortex. There are also sustained firing and transient firing visual cortical cells (Ikeda& Wright 1974). Figure 2 shows that, (1) the highest visual acuity is provided by sustained retinal ganglion cells in the area centralis, sustained cells in the LGN and sustained visual cortical cells which receive inputs from the area
378
H. Ikcda
Retinal ganglion celis
LGN & area 17 calls
Sustained - X
0
5
10
15
20
Sustained - X
25
30 35 40 0 Eccenincity from AC {degrees!
5
10
15
20
25
30
F I G U R E 2. The cellular visual acuity of sustained (a) and transient (b) retinal ganglion cells and sustained (c) and transient (d) LGN cells as a function of retinal eccentricity. The crosses in figures cand d indicate the cellular acuity of visual cortical cells in area 17 which were classified as sustained or transient according to similar criteria to those u.sed in classifying the retinal ganglion cells. The cellular acuit> is expressed as the finest graling (grating of highest spatial frequency expressed in cycles per degree) to which the cell responded
centralis, (2) transient cells have a lower visual acuity than sustained cells in a!l stations of the visual system and (3) there is no significant difference between the highest visual acuity achieved by retina! ganglion cells, LGN cells or visual cortical cells. We may then conclude that the physiological basis of high visual acuity is provided by sustained retinal ganglion cells in the area centralis, the equivalent to the human fovea. 2 Does the function of cells which provide high ri.sual acuity develop postnalally? The answer to this question is 'yes\ This is not surprising if the developmental events occurring postnatally in the visual system of the cat are considered, e.g. optic nerve myelination (Moore et al. 1976), retinal anatomical organization (Donovan 1966, Vogel 1978), synaptie organiza-
Development of visual acuity in kittens
379
tion of LGN cells and cortex {Cragg 1975) and optical quality ofthe eye (Bonds & Freeman 1978) which are not complete at birth. Since it is the sustained cells of the area centralis which provide high visual acuity, in the author's study ofthe development of cellular acuity, it was decided to concentrate on sustained cells in the LGN (Ikeda & Tremain 1978) and more recently on sustained retinal ganglion cells at the area centralis in kittens of different ages (Ikeda & Tremain, present study—see Figure 5). Figure 3 shows the mean (and SE) acuity obtained from sustained LGN cells which received a projection from the area centralis in kittens of ditTerent ages. The acuity ofthe cells develops postnatally, taking up the whole of the time which has been shown as the sensitive period of development for the cat (Hubel & Wiesel 1970, Blakemore 1974). The acuity of sustained cells at the age of 4 months is similar (range 3 5c/ - 5 0 c / ) to that in the adult. When compared with developmental curves of visual acuity obtained by different methods, i.e. a method using visually evoked responses (Freeman & Marg 1975) and a behavioural method (Mitchell ct a!. 1976) the agreement was extremely good. This suggested that the basic developmental curve of visual acuity was already determined at the peripheral origin of the visual pathway before the information from the two eyes is mixed (Ikeda & Tremain 1978). What mechanism is then responsible for this development of cellular
.!! 3
^ 2
T
2 Age (months)
3
4
FIGU RE 3. Development of visual acuity of sustained LGN cells receiving an input from the area centralis ofthe retina which is equivalent to the human fovea. The points indicate Ihe mean acuity ( ± standard error) obtained from 20-30 cells at each age poinl
380
//. Ikcda
visual acuity? The receptive field of the immature sustained retinal ganglion cell has a weak, widespread and ill-detined excitatory centre and a weak, widespread and ill-defined inhibitory surround. Such a receptive field gradually sharpens its excitatory and inhibitory profiles during development atid becomes mature; this is characterized by a tiarrowly and sharply-defined excitatory centre and a strong narrowly-defined inhibitory surround. This is shown diagrammatically in Figure 4. Thus the development of visual acuity is associated with the development of a strong inhibitory surround in sustained retinal ganglion cells in the area centralis. Finally, one can ask. 'Could a physiological mechanism similar to that shown in the cat visual system, govern human high visual acuity?' Is the cat a suitable animal model for understanding human visual acuity and its postnatal development? Figure 5 compares the development of visual acuity in cat and man.
\
Acuity
high
\
low
F I G U R E 4. Comparison of mature and immature receptive field organisation shown schematically. The immature cells have a weak, widespread, ill-detined excitatory centre and a poorly-defined and weak inhibitory surround resulting in poor spatial resolving power. The mature cells have a strong, narrow, sharply-defined excitatory centre and a strong sharply-defined, narrow inhibitory surround suitable for high spatial resolution. i.e. high visual acuity
Development of visual acuity in kittetis
381
12-
10
6 8 Age (months)
10
12
F I G U R E 5. Development of behaviourally measured visual acuity. Comparison of developmental curves of visual acuity hehaviouriiUy determined for cat (Mitchell vt al. 1^76) and man (Gwiazda fi al. 1978). The development of the cat's acuity is complete within ahout 4 months, whereas that of man is still incomplete at 12 months. The squares indicate visual acuity, measured neurophysiologically. of sustained cells from the area centralis in the cat (our work). Whether the cat is a suitable animal model for understanding human visual acuity and its post-natal development is discussed in the texi. Kvy\ cat (Mitchell ('/«/. 1976). man (Gwiazda era/. 1976). • sustained cells (ikeda& Tremain. present results) '
Both curves were determined by behavioural methods, using gratings as used for single neurons. The cat's acuity at maturation was 5c, (about 6 minutes of arc line resolution) and this was considerably poorer than human adult acuity of 30e/ (about I minute of arc line resolution). This was expected from the neuroanatomical point. The high acuity of the human fovea has always been correlated with the packing of foveal cones, i.e. 150 000 eones/mm-. The density of eones in the area centralis of the cat is 25 000 cones/mm-, i.e. about 1/6 of that in man. It is a point of interest that the human acuity is I minute of arc and that of the cat, about
382
H. Ikeda
6 minutes of arc. In the cat. which has a life span of 14-15 years, development appears to be complete at the age of 3 4 months, and as shown by the same points on the dotted eurve in Figure 5. the basic developmental curve is determined by the sustained retinal ganglion cells in the area centralis. However, the eurve for man obtained by Gwiazda ei al. (1978) suggests that the visual acuity is still improving at the age of I year (the acuity of a 1-year-oId is about 12e/\ about 2-5 minutes of arc line resolution), while that of adult is about 30e/ . This is not surprising, because in the eat optic nerve myelination is not complete until 2\ months after birth and visual acuity matures at 3 months. By analogy with the cat, one would predict that the development of human visual acuity would not be complete until at least 2 years, which is the time shown as the completion of optic nerve myelination in man (Friede & Hu 1967) or the LGN anatomy (Hickey 1977). It has been shown that in the cat, form deprivation—habitual blurred image, at the area eentralis due to high refraetive error, squint or nystagmus during the early critical period affects the development of high visual acuity and leads to amblyopia (Ikeda & Tremain 1979). Similarly, any biochemical abnormality or nutritional deficiency present during this critical period would disrupt the development of eells whieh provide high visual acuity and thus affect the development of visual acuity. Again the importance of care in early postnatal life is emphasized. Acknowledgement The experiments described in this paper were carried out in collaboration with Dr K. E. Tremain and the work is supported by the Medical Research Council. REFERENCES Bishop P.O.. Kozak W. & Vakkur G.J. (1962) Some quantitative aspects of the cat's eyes: axis and plane of reference, visual field coordinates and optics. Journal of Physiology 163,456-502 Blakemore C. (1974) Development of functional connections in the mammalian visual system. British Medical Bulletin 30, 152-157 Bonds A.B. & Freeman R.D. (1978) Development of optical quality in Ihe kitten eye, Vi.sion Research 18, 391-398 Boycott B.B. & Wassle H. (1974) The morphological types of ganglion cells of the domestic cat's retina. Journut of Physiology 240. 397-419 Cleland B.G.. Duhin M.W, & Levick W.R. (1971) Sustained and transient neurones in the cat retina and lateral geniculate nucleus. Journal of Physiology 217, 473-497 Cragg B.G. (1975) The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147-166
Development of visual acuity in kittens
383
Donovan A. (1966) The postnatal development of the cat retina. Experimental Eye Re.-ieurch 5, 249 254
Enroth-Cugell C. & Robson J.G. (1966) The contrast sensitivity of retinal ganglion cellsof the cat. Journal of Phy.iiotogy 187. 517 552 Freeman D N . & Marg E. (1975) Visual acuity development coincides with the sensitive period in kittens, Nanire 2S4, 614-615 Friede R.L. & Hu K.H. (1967) Proximo-distal differences in myelin development in human optic nerve fihres. Zeitschrifi fur Zellfor.uhung 79, 259-264 Fukada Y. (1971) Receptive field organisation of cat optic nerve fibres with a special reference to conduction velocily. I'i.sion Re.seanh II. 209-226 Gwiazda J.. Brill S.. Mohindra I. & Held R- (1978) Infant visual acuity and its meridional variation. Vision Research 18, 1557 1564 Hickey T.L. (1977) Postnatal development of the human lateral geniculate nucleus: relationship to a critical period for the visual system. Science 198, 836-838 Hubel D.H. & Wiesel T.N. (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology 206, 419-436 Hughes A. (1974) A quantitative analysis of the cat retinal ganglion cell topography. Jourmd of Comparative .Neurology 163 107 128 lkcda H. & Tremain K.E. (1978) The development of spatial resolving power of lateral geniculate neurones in kittens. Experimental Brain Research 31, 193-206 lkcda H. & Tremain K.E. (1979) Amblyopia occurs in retinal ganglion cells in cats reared with convergent squint without alternating fixation. Experimental Bruin Research 35, 559-582 Ikeda H, & Wright M.J, (1972) Receptive field organisation of "sustained' and "transient' retina! ganglion cells which subserve different functional roles. Journalof Physiology 227, 769-800 Ikeda H. & Wright M.J. (1974) Evidence for "sustained" and 'transient' neurones in the cat's visual cortex. Vi.sion Research 14, 133-136 lkcda H. & Wright M.J. (1976) Properties of LGN cells in kittens reared with convergent squint: a neurophysiological demonstration of amblyopia. Experimental Brain Research 25,63-77 KulIlerS.W.( 1953) Discharge patterns and functional organisation of mammalian retina. Journal of Neurophysiology 16, 37-68 Mitchell DE.. Griffin F.. Wilkinson F.. Anderson P. & Smith M,L, (1976) Visual resolution in young kittens. Vision Research 16. 363 366 Moore C.L,. Kalil R. & Richards W. (1976) Development of myelination in optic tract of the cat. Journal of Comparative Neurology 165, 125-136 Steinberg R.H.. Reid M. & Lacy P.L. (1973) The distribution of rods and cones in the retina of the cat {Feiis domesticus). Journal of Comparative Neurology 148, 229 248 Stone J, (1965) A quantitative analysis of the distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 124, 337-352 Vogel M, (1978) Postnatal development of the cat's retina: a concept of maturation obtained by quantitative and qualitative examinations. Albrecht v. Graefes Archuv fur klini.iche und experimentelle Ophthalmologic 208,93-107
PHYSIOLOGICAL BASIS OF VISUAL ACUITY AND ITS DEVELOPMENT IN KITTENS
H. IKEDA The Rayne Institute, St Thomas's Hospital, London Accepted for publication 16 July 1979
Summary To answer the questions, (1) Which cells in the visual system arc responsible for high visual acuity and (2) Does the function of the cells which provide high visual acuity develop postnatally; single cell studies have been made in the retina, lateral geniculate nucleus (LGN) and visual cortex of cats of different ages. Sustained-X retinal ganglion cells in the area centralis (the equivalent retinal position to the human fovea) set the upper limit of visual acuity. The cellular acuity develops postnatally until it reaches the adult level at 3-4 months-of-age. The improvement of acuity is associated with an increase in the strength of the inhibitory surround mechanism of the receptive field of sustained cells in the area centralis. The maturation of cellular acuity coincides with maturation ol retinal and LGN synaptic organisation and of optic nerve myelination. Visual acuity is an important function of the fovea, the part of the retina which receives the image of an object on which the eye fixates. It is a measure of the minimum detectable angle between two points. Two questions have been asked regarding the physiological basis of visual acuity, using the cat as an animal model. The cat fixates with the area centralis, the area free from blood vessels in the retina where the density of cones and retinal ganglion cells is highest, as in man (Bishop et al. 1962, Steinberg et al. 1973, Stone 1965, Hughes 1974). The two questions are: (1) Which cells in the visual system are responsible for providing the physiological basis for high visual acuity in the mature visual system? (2) Does the function of the cells which provide high visual acuity develop postnatally? I Which cells in the li.sual .system provide rhe physiological basis for high visual acuity? Although without properly functioning cones there can be no high visual 0305-1862/79/1200-037552.00
© 1979 Blackwell Scientific Publications
375
376
H. Ikcda
acuity, visual acuity is the minimum detectable angle between points on a contrasting background and ihus involves the detection of fine contrast. The first cells in the visual system which show such a function clearly are the retitial ganglion cells (Kuffler 1953). We need neurons which respond to stimuli brighter than background in order to see a while letter on a grey background, which are on-centre cells in neurophysiological classification. We also need neurons which respond to stimuli darker than background, which are off-centre cells in neurophysiological classification, in order to see a black letter on a white background. Indeed the on-centre and ofT-centre retinal ganglion cells may provide the physiological basis for contrast detection necessary for visual acuity. But is a specific cell type needed, whether on-cenire or otT-centre. in order to see a very small object, thus achieving high visual acuity? The answer appears to be 'yes'. Neurophysiological studies of retinal ganglion cells and cells in the afferent visual pathway have suggested parallel processing of two aspects of visual information, i.e. spatial discrimination and rapid movement detection, which are initiated from two major types of retinal ganglion cells, regardless of whether the cell is on-centre or ofT-centre (EnrothCugell&Robson !966.Fukada l97I.CleIande/fl/. 1971, Ikeda& Wright 1972). The two types are 'sustained" or 'X' cells and 'transient" or 'Y' cells. As the names suggest, sustained cells are those cells which respond with sustained firing to a stationary stimulus as long as the stimulus is within the receptive field of the cell, while transient cells are those which give only transient firing when the stimulus is presented, but ignore the stimulus soon afterwards. As Figure I illustrates, sustained cells have been identified as beta cells morphologically and have a small cell body and small dendritic field, while transient cells are alpha cells and have a large cell body and large dendritic field (Boycott & Wassle 1974). Sustained cells have very small receptive fields and strong inhibitory surrounds which is the property of linear spatial summation and many other characteristics which are suitable for spatial analysis, while transient cells have properties which are suitable for detection of rapid and coarse movement and initiation of the fixation reflex (Ikeda & Wright 1972). These findings led to the suggestion that it is the 'sustained-X' cell that provides the physiological basis for high visual acuity. This suggestion has been confirmed by experiments in which the visual acuity of individual cells was measured using slowly moving sinusoidal gratings of different line widths, starting from very coarse gratings and gradually challenging the cell with progressively finer gratings. The visual acuity of
Development of visual acuity in kittens
377
Which cell? ANATOMICAL CLASS
PHYSIOLOGICAL CLASS
Alpha cell
(by response to steady stimulus} Transient- Y (Stimulus size I
2.0=
FUNCTIONAL ROLE
Deteclion of rapid movement Initiation of fixation reflex
spikes/sec SuslQined-x Beta cell
[
(Stimulus size • 0.
oi-
Spatial discriminotlon Visual acuity Contrast sensitivity
20 sec.
StimulusJ
On
n
Off
F I G U R E 1. Two major physiological lypes of retinal ganglion cells (transient-Y and suslained-X) correlated with the morphological classificalion of BoycoU and Wiissle (1974) atid their tiring patiern lo an optimal stimulus spot at the receptive field centre. The size of the optimal stimulus, i.e. the stimulus which produces the best response from the cell, is different for transient and sustained cells. Visualacuity is produced by sustained-X cells, morphologically the beta cell
a ceil can be defined as the finest grating to which the cell responds by firing to the individual lines: in other words "recognising* the lines. Measurements of cellular visual acuity have been made in retinal ganglion cells, in cells of layers A and Al ofthe lateral geniculate nucleus (LGN) and in cells of area 17 ofthe visual cortex in normal adult cats, under general anaesthesia. The method and the conditions of measurement have been described in detail elsewhere (Ikcda & Wright 1976). In Figure 2 the visual acuity of sustained retinal ganglion cells (a), transient retinal ganglion cells (b), sustained LGN cells (c) and transient LGN cells (d) is expressed in terms ofthe spatial frequency of a grating, i.e. thenumberof black and white lines in 1 degree of visual angle, which can be resolved by cells, plotted against the retitial eccentricity. The crosses in Figure 2 c and d were obtained from cells in the visual cortex. There are also sustained firing and transient firing visual cortical cells (Ikeda& Wright 1974). Figure 2 shows that, (1) the highest visual acuity is provided by sustained retinal ganglion cells in the area centralis, sustained cells in the LGN and sustained visual cortical cells which receive inputs from the area
378
H. Ikcda
Retinal ganglion celis
LGN & area 17 calls
Sustained - X
0
5
10
15
20
Sustained - X
25
30 35 40 0 Eccenincity from AC {degrees!
5
10
15
20
25
30
F I G U R E 2. The cellular visual acuity of sustained (a) and transient (b) retinal ganglion cells and sustained (c) and transient (d) LGN cells as a function of retinal eccentricity. The crosses in figures cand d indicate the cellular acuity of visual cortical cells in area 17 which were classified as sustained or transient according to similar criteria to those u.sed in classifying the retinal ganglion cells. The cellular acuit> is expressed as the finest graling (grating of highest spatial frequency expressed in cycles per degree) to which the cell responded
centralis, (2) transient cells have a lower visual acuity than sustained cells in a!l stations of the visual system and (3) there is no significant difference between the highest visual acuity achieved by retina! ganglion cells, LGN cells or visual cortical cells. We may then conclude that the physiological basis of high visual acuity is provided by sustained retinal ganglion cells in the area centralis, the equivalent to the human fovea. 2 Does the function of cells which provide high ri.sual acuity develop postnalally? The answer to this question is 'yes\ This is not surprising if the developmental events occurring postnatally in the visual system of the cat are considered, e.g. optic nerve myelination (Moore et al. 1976), retinal anatomical organization (Donovan 1966, Vogel 1978), synaptie organiza-
Development of visual acuity in kittens
379
tion of LGN cells and cortex {Cragg 1975) and optical quality ofthe eye (Bonds & Freeman 1978) which are not complete at birth. Since it is the sustained cells of the area centralis which provide high visual acuity, in the author's study ofthe development of cellular acuity, it was decided to concentrate on sustained cells in the LGN (Ikeda & Tremain 1978) and more recently on sustained retinal ganglion cells at the area centralis in kittens of different ages (Ikeda & Tremain, present study—see Figure 5). Figure 3 shows the mean (and SE) acuity obtained from sustained LGN cells which received a projection from the area centralis in kittens of ditTerent ages. The acuity ofthe cells develops postnatally, taking up the whole of the time which has been shown as the sensitive period of development for the cat (Hubel & Wiesel 1970, Blakemore 1974). The acuity of sustained cells at the age of 4 months is similar (range 3 5c/ - 5 0 c / ) to that in the adult. When compared with developmental curves of visual acuity obtained by different methods, i.e. a method using visually evoked responses (Freeman & Marg 1975) and a behavioural method (Mitchell ct a!. 1976) the agreement was extremely good. This suggested that the basic developmental curve of visual acuity was already determined at the peripheral origin of the visual pathway before the information from the two eyes is mixed (Ikeda & Tremain 1978). What mechanism is then responsible for this development of cellular
.!! 3
^ 2
T
2 Age (months)
3
4
FIGU RE 3. Development of visual acuity of sustained LGN cells receiving an input from the area centralis ofthe retina which is equivalent to the human fovea. The points indicate Ihe mean acuity ( ± standard error) obtained from 20-30 cells at each age poinl
380
//. Ikcda
visual acuity? The receptive field of the immature sustained retinal ganglion cell has a weak, widespread and ill-detined excitatory centre and a weak, widespread and ill-defined inhibitory surround. Such a receptive field gradually sharpens its excitatory and inhibitory profiles during development atid becomes mature; this is characterized by a tiarrowly and sharply-defined excitatory centre and a strong narrowly-defined inhibitory surround. This is shown diagrammatically in Figure 4. Thus the development of visual acuity is associated with the development of a strong inhibitory surround in sustained retinal ganglion cells in the area centralis. Finally, one can ask. 'Could a physiological mechanism similar to that shown in the cat visual system, govern human high visual acuity?' Is the cat a suitable animal model for understanding human visual acuity and its postnatal development? Figure 5 compares the development of visual acuity in cat and man.
\
Acuity
high
\
low
F I G U R E 4. Comparison of mature and immature receptive field organisation shown schematically. The immature cells have a weak, widespread, ill-detined excitatory centre and a poorly-defined and weak inhibitory surround resulting in poor spatial resolving power. The mature cells have a strong, narrow, sharply-defined excitatory centre and a strong sharply-defined, narrow inhibitory surround suitable for high spatial resolution. i.e. high visual acuity
Development of visual acuity in kittetis
381
12-
10
6 8 Age (months)
10
12
F I G U R E 5. Development of behaviourally measured visual acuity. Comparison of developmental curves of visual acuity hehaviouriiUy determined for cat (Mitchell vt al. 1^76) and man (Gwiazda fi al. 1978). The development of the cat's acuity is complete within ahout 4 months, whereas that of man is still incomplete at 12 months. The squares indicate visual acuity, measured neurophysiologically. of sustained cells from the area centralis in the cat (our work). Whether the cat is a suitable animal model for understanding human visual acuity and its post-natal development is discussed in the texi. Kvy\ cat (Mitchell ('/«/. 1976). man (Gwiazda era/. 1976). • sustained cells (ikeda& Tremain. present results) '
Both curves were determined by behavioural methods, using gratings as used for single neurons. The cat's acuity at maturation was 5c, (about 6 minutes of arc line resolution) and this was considerably poorer than human adult acuity of 30e/ (about I minute of arc line resolution). This was expected from the neuroanatomical point. The high acuity of the human fovea has always been correlated with the packing of foveal cones, i.e. 150 000 eones/mm-. The density of eones in the area centralis of the cat is 25 000 cones/mm-, i.e. about 1/6 of that in man. It is a point of interest that the human acuity is I minute of arc and that of the cat, about
382
H. Ikeda
6 minutes of arc. In the cat. which has a life span of 14-15 years, development appears to be complete at the age of 3 4 months, and as shown by the same points on the dotted eurve in Figure 5. the basic developmental curve is determined by the sustained retinal ganglion cells in the area centralis. However, the eurve for man obtained by Gwiazda ei al. (1978) suggests that the visual acuity is still improving at the age of I year (the acuity of a 1-year-oId is about 12e/\ about 2-5 minutes of arc line resolution), while that of adult is about 30e/ . This is not surprising, because in the eat optic nerve myelination is not complete until 2\ months after birth and visual acuity matures at 3 months. By analogy with the cat, one would predict that the development of human visual acuity would not be complete until at least 2 years, which is the time shown as the completion of optic nerve myelination in man (Friede & Hu 1967) or the LGN anatomy (Hickey 1977). It has been shown that in the cat, form deprivation—habitual blurred image, at the area eentralis due to high refraetive error, squint or nystagmus during the early critical period affects the development of high visual acuity and leads to amblyopia (Ikeda & Tremain 1979). Similarly, any biochemical abnormality or nutritional deficiency present during this critical period would disrupt the development of eells whieh provide high visual acuity and thus affect the development of visual acuity. Again the importance of care in early postnatal life is emphasized. Acknowledgement The experiments described in this paper were carried out in collaboration with Dr K. E. Tremain and the work is supported by the Medical Research Council. REFERENCES Bishop P.O.. Kozak W. & Vakkur G.J. (1962) Some quantitative aspects of the cat's eyes: axis and plane of reference, visual field coordinates and optics. Journal of Physiology 163,456-502 Blakemore C. (1974) Development of functional connections in the mammalian visual system. British Medical Bulletin 30, 152-157 Bonds A.B. & Freeman R.D. (1978) Development of optical quality in Ihe kitten eye, Vi.sion Research 18, 391-398 Boycott B.B. & Wassle H. (1974) The morphological types of ganglion cells of the domestic cat's retina. Journut of Physiology 240. 397-419 Cleland B.G.. Duhin M.W, & Levick W.R. (1971) Sustained and transient neurones in the cat retina and lateral geniculate nucleus. Journal of Physiology 217, 473-497 Cragg B.G. (1975) The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147-166
Development of visual acuity in kittens
383
Donovan A. (1966) The postnatal development of the cat retina. Experimental Eye Re.-ieurch 5, 249 254
Enroth-Cugell C. & Robson J.G. (1966) The contrast sensitivity of retinal ganglion cellsof the cat. Journal of Phy.iiotogy 187. 517 552 Freeman D N . & Marg E. (1975) Visual acuity development coincides with the sensitive period in kittens, Nanire 2S4, 614-615 Friede R.L. & Hu K.H. (1967) Proximo-distal differences in myelin development in human optic nerve fihres. Zeitschrifi fur Zellfor.uhung 79, 259-264 Fukada Y. (1971) Receptive field organisation of cat optic nerve fibres with a special reference to conduction velocily. I'i.sion Re.seanh II. 209-226 Gwiazda J.. Brill S.. Mohindra I. & Held R- (1978) Infant visual acuity and its meridional variation. Vision Research 18, 1557 1564 Hickey T.L. (1977) Postnatal development of the human lateral geniculate nucleus: relationship to a critical period for the visual system. Science 198, 836-838 Hubel D.H. & Wiesel T.N. (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology 206, 419-436 Hughes A. (1974) A quantitative analysis of the cat retinal ganglion cell topography. Jourmd of Comparative .Neurology 163 107 128 lkcda H. & Tremain K.E. (1978) The development of spatial resolving power of lateral geniculate neurones in kittens. Experimental Brain Research 31, 193-206 lkcda H. & Tremain K.E. (1979) Amblyopia occurs in retinal ganglion cells in cats reared with convergent squint without alternating fixation. Experimental Bruin Research 35, 559-582 Ikeda H, & Wright M.J, (1972) Receptive field organisation of "sustained' and "transient' retina! ganglion cells which subserve different functional roles. Journalof Physiology 227, 769-800 Ikeda H. & Wright M.J. (1974) Evidence for "sustained" and 'transient' neurones in the cat's visual cortex. Vi.sion Research 14, 133-136 lkcda H. & Wright M.J. (1976) Properties of LGN cells in kittens reared with convergent squint: a neurophysiological demonstration of amblyopia. Experimental Brain Research 25,63-77 KulIlerS.W.( 1953) Discharge patterns and functional organisation of mammalian retina. Journal of Neurophysiology 16, 37-68 Mitchell DE.. Griffin F.. Wilkinson F.. Anderson P. & Smith M,L, (1976) Visual resolution in young kittens. Vision Research 16. 363 366 Moore C.L,. Kalil R. & Richards W. (1976) Development of myelination in optic tract of the cat. Journal of Comparative Neurology 165, 125-136 Steinberg R.H.. Reid M. & Lacy P.L. (1973) The distribution of rods and cones in the retina of the cat {Feiis domesticus). Journal of Comparative Neurology 148, 229 248 Stone J, (1965) A quantitative analysis of the distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 124, 337-352 Vogel M, (1978) Postnatal development of the cat's retina: a concept of maturation obtained by quantitative and qualitative examinations. Albrecht v. Graefes Archuv fur klini.iche und experimentelle Ophthalmologic 208,93-107
