A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB

Abstract

The adult cerebral cortex can adapt to environmental change. Using monocular deprivation as a paradigm, we find that rapid experience-dependent plasticity exists even in the mature primary visual cortex. However, adult cortical plasticity differs from developmental plasticity in two important ways. First, the effect of adult, but not juvenile monocular deprivation is strongly suppressed by administration of barbiturate just prior to recording visual evoked potentials, suggesting that the effect of adult experience can be inactivated acutely. Second, the effect of deprivation is less persistent over time in adults than in juveniles. This correlates with the known decline in CREB function during maturation of the visual cortex. To compensate for this decline in CREB function, we expressed persistently active VP16-CREB and find that it causes adult plasticity to become persistent. These results suggest that in development and adulthood, the regulation of a trans-synaptic signaling pathway controls the adaptive potential of cortical circuits.A primary function of the brain is to integrate the individual into a continually changing environment. Some aspects of this integration are accomplished through developmental processes, other aspects through learning. Although learning can occur throughout life, many behaviors, from language to sexual behavior, are shaped profoundly by early life experience. In this study, we have examined how the adaptive capacity of the cerebral cortex changes with maturation.A classical model of developmental plasticity is ocular dominance plasticity (Wiesel and Hubel 1963;Hubel and Wiesel 1998). Hubel and Wiesel showed that closing one eye of an infant cat produced a visual cortex dominated by the nondeprived eye. Closing an eye of an adult cat was ineffective. Single-unit studies in a number of mammalian systems, ranging from rodents to primates, have found that ocular dominance plasticity is restricted to a period prior to puberty (Hubel and Wiesel 1970;Blakemore et al. 1978;Olson and Freeman 1980;Issa et al. 1999;Fagiolini and Hensch 2000). The amount of deprivation required to alter the responses of visual cortical neurons depends on the animal's age. In the cat, during the peak of the critical period (4-5 wk of age), as little as 1 d of deprivation is sufficient to cause ocular dominance changes (Olson and Freeman 1975). Near the age of puberty, weeks or months of deprivation are necessary to induce changes observable by single-unit recordings, and the changes are thought to occur only in layers 2 and 3 of the visual cortex (Daw et al. 1992).In the clinical literature, however, there are reports suggesting that improvement of visual acuity can occur in adult patients with amblyopia, a central disorder of visual acuity, following patching of the normal eye (Selenow and Ciuffreda 1986; Saulles 1987; Rutstein and Fuhr 1992; Wick and Wingard 1992). Furthermore, a lengthy period of monocular occlusion caused by a dense cataract (Sloper and Collins 1995) can cause significant changes in visu...

Rapid recovery from the effects of early monocular deprivation is enabled by temporary inactivation of the retinas

“…However, one unusual feature of mouse ocular dominance plasticity is that it persists well into adulthood (42), particularly when visual experience is enriched (49,50). An additional complication is that the ocular dominance shift initiated in adults reverts spontaneously when binocular vision is restored (51,52) or if both eyelids are closed (53). Thus, for the mouse to serve as a useful model for amblyopia following early-life MD, it was of particular importance to understand the degree to which the juvenile ocular dominance shift persists when binocular experience is restored.…”

Visual Deprivation Modifies Both Presynaptic Glutamate Release and the Composition of Perisynaptic/Extrasynaptic NMDA Receptors in Adult Visual Cortex

“…For example, monocular deprivation shifts the ocular dominance of neurons in the primary visual cortex of adult mice, although the manner of the shift differs from that observed in juveniles (Sawtell et al, 2003;Frenkel and Bear, 2004;Pham et al, 2004). In juvenile mice monocular deprivation causes a rapid reduction of the deprived eye response recorded in the contralateral cortex, followed by a potentiation of the responses driven by the nondeprived eye in the ipsilateral cortex.…”

Laminar-Specific Maturation of GABAergic Transmission and Susceptibility to Visual Deprivation Are Related to Endocannabinoid Sensitivity in Mouse Visual Cortex

“…In fact, it was reported that the effect of monocular deprivation starts and terminates earlier in layer 4 than in other layers of the cat visual cortex (Daw et al, 1992), and ocular dominance plasticity in layer 4 is much weaker than that in extragranular layers of the mouse visual cortex (Gordon and Stryker, 1996). Furthermore, in layer 2/3 of the cortex, the ocular dominance plasticity remains to a substantial extent in juvenile or even fully mature animals (Daw et al, 1992;Guire et al, 1999;Sawtell et al, 2003;Pham et al, 2004;Sato and Stryker, 2008).…”