scholarly journals The critical period: neurochemical and synaptic mechanisms shared by the visual cortex and the brain stem respiratory system

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.

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.


2009 ◽  
Vol 3 (3) ◽  
pp. 222-227 ◽  
Author(s):  
Maria Vania Silva Nunes ◽  
Alexandre Castro-Caldas ◽  
Dolores Del Rio ◽  
Fernado Maestú ◽  
Tomás Ortiz

Abstract The lifelong acquisition of cognitive skills shapes the biology of the brain. However, there are critical periods for the best use of the brain to process the acquired information. Objectives: To discuss the critical period of cognitive acquisition, the concept of cognitive reserve and the HAROLD (Hemispheric Asymmetry Reduction in Older adults) model. Methods: Seven women who learned how to read and to write after the age of 50 (ex-illiterates) and five women with 10 years of regular schooling (controls) were submitted to a language recognition test while brain activity was being recorded using magnetoencephalography. Spoken words were delivered binaurally via two plastic tubs terminating in ear inserts, and recordings were made with a whole head magnetometer consisting of 148 magnetometer coils. Results: Both groups performed similarly on the task of identifying target words. Analysis of the number of sources of activity in the left and right hemispheres revealed significant differences between the two groups, showing that ex-illiterate subjects exhibited less brain functional asymmetry during the language task. Conclusions: These results should be interpreted with caution because the groups were small. However, these findings reinforce the concept that poorly educated subjects tend to use the brain for information processing in a different way to subjects with a high educational level or who were schooled at the regular time. Finally, the recruiting of both hemispheres to tackle the language recognition test occurred to a greater degree in the ex-illiterate group where this can be interpreted as a sign of difficulty performing the task.


2022 ◽  
Author(s):  
Andrea Kóbor ◽  
Karolina Janacsek ◽  
Petra Hermann ◽  
Zsofia Zavecz ◽  
Vera Varga ◽  
...  

Previous research recognized that humans could extract statistical regularities of the environment to automatically predict upcoming events. However, it has remained unexplored how the brain encodes the distribution of statistical regularities if it continuously changes. To investigate this question, we devised an fMRI paradigm where participants (N = 32) completed a visual four-choice reaction time (RT) task consisting of statistical regularities. Two types of blocks involving the same perceptual elements alternated with one another throughout the task: While the distribution of statistical regularities was predictable in one block type, it was unpredictable in the other. Participants were unaware of the presence of statistical regularities and of their changing distribution across the subsequent task blocks. Based on the RT results, although statistical regularities were processed similarly in both the predictable and unpredictable blocks, participants acquired less statistical knowledge in the unpredictable as compared with the predictable blocks. Whole-brain random-effects analyses showed increased activity in the early visual cortex and decreased activity in the precuneus for the predictable as compared with the unpredictable blocks. Therefore, the actual predictability of statistical regularities is likely to be represented already at the early stages of visual cortical processing. However, decreased precuneus activity suggests that these representations are imperfectly updated to track the multiple shifts in predictability throughout the task. The results also highlight that the processing of statistical regularities in a changing environment could be habitual.


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.


1971 ◽  
Vol 11 ◽  
pp. 104-105
Author(s):  
Tadahisa KURIMOTO ◽  
Kentaro KOSHINO ◽  
Kuniyuki SOMEDA ◽  
Satoru KUBOTA ◽  
Takayuki NAKAJIMA ◽  
...  

PLoS Biology ◽  
2020 ◽  
Vol 18 (11) ◽  
pp. e3000921
Author(s):  
Zvi N. Roth ◽  
Minyoung Ryoo ◽  
Elisha P. Merriam

The brain exhibits widespread endogenous responses in the absence of visual stimuli, even at the earliest stages of visual cortical processing. Such responses have been studied in monkeys using optical imaging with a limited field of view over visual cortex. Here, we used functional MRI (fMRI) in human participants to study the link between arousal and endogenous responses in visual cortex. The response that we observed was tightly entrained to task timing, was spatially extensive, and was independent of visual stimulation. We found that this response follows dynamics similar to that of pupil size and heart rate, suggesting that task-related activity is related to arousal. Finally, we found that higher reward increased response amplitude while decreasing its trial-to-trial variability (i.e., the noise). Computational simulations suggest that increased temporal precision underlies both of these observations. Our findings are consistent with optical imaging studies in monkeys and support the notion that arousal increases precision of neural activity.


1992 ◽  
Vol 160 (5) ◽  
pp. 659-663 ◽  
Author(s):  
R. J. McClelland ◽  
D. G. Eyre ◽  
D. Watson ◽  
G. J. Calvert ◽  
Eileen Sherrard

To investigate the integrity of the brain-stem in 20 mentally handicapped children who met the Rutter criteria for autism, brain-stem auditory evoked potentials were obtained for a range of stimulus intensities. Central conduction times (CCTs) were calculated for the Wave l–Wave V interval of the brain-stem potentials. In children under 14 years of age CCTs were normal. In children 14 years of age and over, three of four girls and eight of nine boys had CCTs exceeding normal limits when compared with a group of controls of normal intelligence, matched for age and sex. CCTs recorded from a group of non-autistic mentally handicapped children were within normal limits. The age distributions are consistent with a maturational defect in myelination within the brain-stem in autism, a defect which may have a much wider anatomical distribution throughout cortical and subcortical structures.


2018 ◽  
Author(s):  
Adema Ribic ◽  
Michael C. Crair ◽  
Thomas Biederer

HighlightsThe synaptogenic molecule SynCAM 1 is selectively regulated by visual experienceSynCAM 1 controls thalamic input onto cortical Parvalbumin (PV+) interneuronsPV+-specific knockdown of SynCAM 1 arrests maturation of cortical inhibitionThalamic excitation onto PV+ interneurons is essential for critical period closureeTOC BlurbRibic et al. show that network plasticity in both young and adult cortex is restricted by the synapse organizing molecule SynCAM 1. On a cellular level, it functions in Parvalbumin-positive interneurons to recruit thalamocortical terminals. This controls the maturation of inhibitory drive and restricts plasticity in the cortex. These results reveal the synaptic locus of cortical plasticity and identify the first cell-autonomous synaptic factor for closure of cortical critical periods.SummaryBrain plasticity peaks early in life and tapers in adulthood. This is exemplified in the primary visual cortex, where brief loss of vision to one eye abrogates cortical responses to inputs from that eye during the critical period, but not in adulthood. The synaptic locus of critical period plasticity and the cell-autonomous synaptic factors timing these periods remain unclear. We here demonstrate that the immunoglobulin protein Synaptic Cell Adhesion Molecule 1 (SynCAM 1/Cadm1) is regulated by visual experience and limits visual cortex plasticity. SynCAM 1 selectively controls the number of excitatory thalamocortical (TC) inputs onto Parvalbumin (PV+) interneurons and loss of SynCAM 1 in turn impairs the maturation of TC-driven feed-forward inhibition. SynCAM 1 acts in cortical PV+ interneurons to perform these functions and its PV+-specific knockdown prevents the age-related plasticity decline. These results identify a synapse type-specific, cell-autonomous mechanism that governs circuit maturation and closes the visual critical period.


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