Critical periods for functional and anatomical compensation in lateral suprasylvian visual area following removal of visual cortex in cats

1984 ◽  
Vol 52 (5) ◽  
pp. 941-960 ◽  
Author(s):  
L. Tong ◽  
R. E. Kalil ◽  
P. D. Spear

Previous experiments have found that neurons in the cat's lateral suprasylvian (LS) visual area of cortex show functional compensation following removal of visual cortical areas 17, 18, and 19 on the day of birth. Correspondingly, an enhanced retino-thalamic pathway to LS cortex develops in these cats. The present experiments investigated the critical periods for these changes. Unilateral lesions of areas 17, 18, and 19 were made in cats ranging in age from 1 day postnatal to 26 wk. When the cats were adult, single-cell recordings were made from LS cortex ipsilateral to the lesion. In addition, transneuronal autoradiographic methods were used to trace the retino-thalamic projections to LS cortex in many of the same animals. Following lesions in 18- and 26-wk-old cats, there is a marked reduction in direction-selective LS cortex cells and an increase in cells that respond best to stationary flashing stimuli. These results are similar to those following visual cortex lesions in adult cats. In contrast, the percentages of cells with these properties are normal following lesions made from 1 day to 12 wk of age. Thus the critical period for development of direction selectivity and greater responses to moving than to stationary flashing stimuli in LS cortex following a visual cortex lesion ends between 12 and 18 wk of age. Following lesions in 26-wk-old cats, there is a decrease in the percentage of cells that respond to the ipsilateral eye, which is similar to results following visual cortex lesions in adult cats. However, ocular dominance is normal following lesions made from 1 day to 18 wk of age. Thus the critical period for development of responses to the ipsilateral eye following a lesion ends between 18 and 26 wk of age. Following visual cortex lesions in 2-, 4-, or 8-wk-old cats, about 30% of the LS cortex cells display orientation selectivity to elongated slits of light. In contrast, few or no cells display this property in normal adult cats, cats with lesions made on the day of birth, or cats with lesions made at 12 wk of age or later. Thus an anomalous property develops for many LS cells, and the critical period for this property begins later (between 1 day and 2 wk) and ends earlier (between 8 and 12 wk) than those for other properties.(ABSTRACT TRUNCATED AT 400 WORDS)

2018 ◽  
Vol 35 ◽  
Author(s):  
TAKAO K. HENSCH ◽  
ELIZABETH M. QUINLAN

AbstractThe shift in ocular dominance (OD) of binocular neurons induced by monocular deprivation is the canonical model of synaptic plasticity confined to a postnatal critical period. Developmental constraints on this plasticity not only lend stability to the mature visual cortical circuitry but also impede the ability to recover from amblyopia beyond an early window. Advances with mouse models utilizing the power of molecular, genetic, and imaging tools are beginning to unravel the circuit, cellular, and molecular mechanisms controlling the onset and closure of the critical periods of plasticity in the primary visual cortex (V1). Emerging evidence suggests that mechanisms enabling plasticity in juveniles are not simply lost with age but rather that plasticity is actively constrained by the developmental up-regulation of molecular ‘brakes’. Lifting these brakes enhances plasticity in the adult visual cortex, and can be harnessed to promote recovery from amblyopia. The reactivation of plasticity by experimental manipulations has revised the idea that robust OD plasticity is limited to early postnatal development. Here, we discuss recent insights into the neurobiology of the initiation and termination of critical periods and how our increasingly mechanistic understanding of these processes can be leveraged toward improved clinical treatment of adult amblyopia.


2015 ◽  
Vol 112 (24) ◽  
pp. E3131-E3140 ◽  
Author(s):  
Xiaojie Huang ◽  
Sophia K. Stodieck ◽  
Bianka Goetze ◽  
Lei Cui ◽  
Man Ho Wong ◽  
...  

During critical periods, all cortical neural circuits are refined to optimize their functional properties. The prevailing notion is that the balance between excitation and inhibition determines the onset and closure of critical periods. In contrast, we show that maturation of silent glutamatergic synapses onto principal neurons was sufficient to govern the duration of the critical period for ocular dominance plasticity in the visual cortex of mice. Specifically, postsynaptic density protein-95 (PSD-95) was absolutely required for experience-dependent maturation of silent synapses, and its absence before the onset of critical periods resulted in lifelong juvenile ocular dominance plasticity. Loss of PSD-95 in the visual cortex after the closure of the critical period reinstated silent synapses, resulting in reopening of juvenile-like ocular dominance plasticity. Additionally, silent synapse-based ocular dominance plasticity was largely independent of the inhibitory tone, whose developmental maturation was independent of PSD-95. Moreover, glutamatergic synaptic transmission onto parvalbumin-positive interneurons was unaltered in PSD-95 KO mice. These findings reveal not only that PSD-95–dependent silent synapse maturation in visual cortical principal neurons terminates the critical period for ocular dominance plasticity but also indicate that, in general, once silent synapses are consolidated in any neural circuit, initial experience-dependent functional optimization and critical periods end.


2002 ◽  
Vol 88 (4) ◽  
pp. 1933-1940 ◽  
Author(s):  
Chris J. Beaver ◽  
Quentin S. Fischer ◽  
Qinghua Ji ◽  
Nigel W. Daw

We have previously shown that the protein kinase A (PKA) inhibitor, 8-chloroadenosine-3′,5′–monophosphorothioate (Rp-8-Cl-cAMPS), abolishes ocular dominance plasticity in the cat visual cortex. Here we investigate the effect of this inhibitor on orientation selectivity. The inhibitor reduces orientation selectivity in monocularly deprived animals but not in normal animals. In other words, PKA inhibitors by themselves do not affect orientation selectivity, nor does monocular deprivation by itself, but monocular deprivation in combination with a PKA inhibitor does affect orientation selectivity. This result is found for the receptive fields in both deprived and nondeprived eyes. Although there is a tendency for the orientation selectivity in the nondeprived eye to be higher than the orientation selectivity in the deprived eye, the orientation selectivity in both eyes is considerably less than normal. The result is striking in animals at 4 wk of age. The effect of the monocular deprivation on orientation selectivity is reduced at 6 wk of age and absent at 9 wk of age, while the effect on ocular dominance shifts is less changed in agreement with previous results showing that the critical period for orientation/direction selectivity ends earlier than the critical period for ocular dominance. We conclude that closure of one eye in combination with inhibition of PKA reduces orientation selectivity during the period that orientation selectivity is still mutable and that the reduction in orientation selectivity is transferred to the nondeprived eye.


1997 ◽  
Vol 14 (1) ◽  
pp. 111-123 ◽  
Author(s):  
Rosita Siciliano ◽  
Gigliola Fontanesi ◽  
Fiorella Casamenti ◽  
Nicoletta Berardi ◽  
Paola Bagnoli ◽  
...  

AbstractIn the rat, visual cortical cells develop their functional properties during a period termed as critical period, which is included between eye opening, i.e.˘postnatal day (PD) 15, and PD40. The present investigation was aimed at studying the influence of cortical cholinergic afferents from the basal forebrain (BF) on the development of functional properties of visual cortical neurons. At PD15, rats were unilaterally deprived of the cholinergic input to the visual cortex by stereotaxic injections of quisqualic acid in BF cholinergic nuclei projecting to the visual cortex. Cortical cell functional properties, such as ocular dominance, orientation selectivity, receptive-field size, and cell responsiveness were then assessed by extracellular recordings in the visual cortex ipsilateral to the lesioned BF both during the critical period (PD30) and after its end (PD45). After the recording session, the rats were sacrificed and the extent of both cholinergic lesion in BF and cholinergic depletion in the visual cortex was determined. Our results show that lesion of BF cholinergic nuclei transiently alters the ocular dominance of visual cortical cells while it does not affect the other functional properties tested. In particular, in lesioned animals recorded during the critical period, a higher percentage of visual cortical cells was driven by the contralateral eye with respect to normal animals. After the end of the critical period, the ocular dominance distribution of animals with cholinergic deafferentation was not significantly different from that of controls. Our results suggest the possibility that lesions of BF cholinergic neurons performed during postnatal development only transiently interfere with cortical competitive processes.


1994 ◽  
Vol 11 (6) ◽  
pp. 1093-1102 ◽  
Author(s):  
Luciano Domenici ◽  
Gigliola Fontanesi ◽  
Antonio Cattaneo ◽  
Paola Bagnoli ◽  
Lamberto Maffei

AbstractRecent investigations have shown that cortical nerve growth factor (NGF) infusions during the critical period inhibit ocular-dominance plasticity in the binocular portion of the rat visual cortex. The mechanisms underlying the effects of NGF on visual cortical plasticity are still unclear. To investigate whether during normal development intracortical and/or extracortical cells possess uptake/transport mechanisms for the neurotrophin, we injected 125I-NGF into the occipital cortex of rats at different postnatal ages. Within the cortex, only a few labelled cells were observed. These cells were confined to the vicinity of the injection site and their number depended on the animal's age at the time of injection. Labelled cells were absent at postnatal day (PD) 10 but could be detected between PD 14 and PD 18. They then decreased in number over the following period and were not detected in adult animals. Outside the cortex, neurons of the lateral geniculate nucleus (LGN) were not observed to take up and retrogradely transport NGF at any age after birth. In contrast, retrogradely labelled neurons were found in the basal forebrain. Labelled cells were first observed here at PD 14 and then increased in number until reaching the adult pattern. Our results show that intrinsic and extrinsic neurons are labelled following intracortical injections of iodinated NGF. In both neuronal populations, the uptake and transport of NGF is present over a period corresponding to the critical period for visual cortical plasticity. These findings suggest that NGF may play a role, both intra and extracortically, in plasticity phenomena.


2018 ◽  
Author(s):  
Anna Steinzeig ◽  
Cecilia Cannarozzo ◽  
Eero Castren

Heightened neuronal plasticity expressed during early postnatal life has been thought to permanently decline once critical periods have ended. For example, monocular deprivation is able to shift ocular dominance in the mouse visual cortex during the first months of life, but this effect is lost later in life. However, various treatments such as the antidepressant fluoxetine can reactivate a critical period-like plasticity in the adult brain. When monocular deprivation is supplemented with chronic fluoxetine administration, a major shift in ocular dominance is produced after the critical period has ended. In the current study, we characterized the temporal patterns of fluoxetine-induced plasticity in the adult mouse visual cortex, using in vivo optical imaging. We found that artificially-induced plasticity in ocular dominance extended beyond the duration of the naturally occurring critical period, and continued as long as fluoxetine was administered. However, this fluoxetine-induced plasticity period ended as soon as the drug was not given. Taken together, our data highlights how a combination of pharmacological treatment and environmental change could be used to improve strategies in antidepressant therapy in humans.


2021 ◽  
Vol 288 (1958) ◽  
pp. 20211025
Author(s):  
Margaret T. T. Wong-Riley

The landmark studies of Wiesel and Hubel in the 1960's initiated a surge of investigations into the critical period of visual cortical development, when abnormal visual experience can alter cortical structures and functions. Most studies focused on the visual cortex, with relatively little attention to subcortical structures. The goal of the present review is to elucidate neurochemical and synaptic mechanisms common to the critical periods of the visual cortex and the brain stem respiratory system in the normal rat. In both regions, the critical period is a time of (i) heightened inhibition; (ii) reduced expression of brain-derived neurotrophic factor (BDNF); and (iii) synaptic imbalance , with heightened inhibition and suppressed excitation. The last two mechanisms are contrary to the conventional premise. Synaptic imbalance renders developing neurons more vulnerable to external stressors. However, the critical period is necessary to enable each system to strengthen its circuitry, adapt to its environment, and transition from immaturity to maturity, when a state of relative synaptic balance is attained. Failure to achieve such a balance leads to neurological disorders.


1992 ◽  
Vol 67 (1) ◽  
pp. 197-202 ◽  
Author(s):  
N. W. Daw ◽  
K. Fox ◽  
H. Sato ◽  
D. Czepita

1. Cats were monocularly deprived for 3 mo starting at 8-9 mo, 12 mo, 15 mo, and several years of age. Single cells were recorded in both visual cortexes of each cat, and the ocular dominance and layer determined for each cell. Ocular dominance histograms were then constructed for layers II/III, IV, and V/VI for each group of animals. 2. There was a statistically significant shift in the ocular dominance for cells in layers II/III and V/VI for the animals deprived between 8-9 and 11-12 mo of age. There was a small but not statistically significant shift for cells in layer IV from the animals deprived between 8-9 and 11-12 mo of age, and for cells in layers V/VI from the animals deprived between 15 and 18 mo of age. There was no noticeable shift in ocular dominance for any other layers in any other group of animals. 3. We conclude that the critical period for monocular deprivation is finally over at approximately 1 yr of age for extragranular layers (layers II, III, V, and VI) in visual cortex of the cat.


2004 ◽  
Vol 92 (5) ◽  
pp. 2947-2959 ◽  
Author(s):  
Miguel Á. Carreira-Perpiñán ◽  
Geoffrey J. Goodhill

Maps of ocular dominance and orientation in primary visual cortex have a highly characteristic structure. The factors that determine this structure are still largely unknown. In particular, it is unclear how short-range excitatory and inhibitory connections between nearby neurons influence structure both within and between maps. Using a generalized version of a well-known computational model of visual cortical map development, we show that the number of excitatory and inhibitory oscillations in this interaction function critically influences map structure. Specifically, we demonstrate that functions that oscillate more than once do not produce maps closely resembling those seen biologically. This strongly suggests that local lateral connections in visual cortex oscillate only once and have the form of a Mexican hat.


1990 ◽  
Vol 64 (4) ◽  
pp. 1352-1360 ◽  
Author(s):  
M. R. Isley ◽  
D. C. Rogers-Ramachandran ◽  
P. G. Shinkman

1. The present experiments were designed to assess the effects of relatively large optically induced interocular torsional disparities on the developing kitten visual cortex. Kittens were reared with restricted visual experience. Three groups viewed a normal visual environment through goggles fitted with small prisms that introduced torsional disparities between the left and right eyes' visual fields, equal but opposite in the two eyes. Kittens in the +32 degrees goggle rearing condition experienced a 16 degrees counterclockwise rotation of the left visual field and a 16 degrees clockwise rotation of the right visual field; in the -32 degrees goggle condition the rotations were clockwise in the left eye and counterclockwise in the right. In the control (0 degree) goggle condition, the prisms did not rotate the visual fields. Three additional groups viewed high-contrast square-wave gratings through Polaroid filters arranged to provide a constant 32 degrees of interocular orientation disparity. 2. Recordings were made from neurons in visual cortex around the border of areas 17 and 18 in all kittens. Development of cortical ocular dominance columns was severely disrupted in all the experimental (rotated) rearing conditions. Most cells were classified in the extreme ocular dominance categories 1, 2, 6, and 7. Development of the system of orientation columns was also affected: among the relatively few cells with oriented receptive fields in both eyes, the distributions of interocular disparities in preferred stimulus orientation were centered near 0 degree but showed significantly larger variances than in the control condition.(ABSTRACT TRUNCATED AT 250 WORDS)


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