Multiple Postsynaptic Protein Levels Are Maintained in a Delayed Form of Compensatory, Experience-Dependent Plasticity in Adult Superior Colliculus

Abstract

AbstractRefinement of developing visual projections is reported to depend on visual experience in rats, cats, ferrets, and monkeys. Visual deprivation in these species delays visual pathway development, reportedly maintaining a juvenile condition and prolonging the critical period for plasticity. Deprivation has been associated with retention of immature NMDA and GABAA receptors and a juvenile state of chloride transporters. In contrast, receptive fields (RFs) in superior colliculus (SC) and visual cortex (V1) of Syrian hamsters refine normally with spontaneous activity alone, requiring visual experience only to maintain refined RFs in adulthood. Continued visual deprivation into adulthood leads to RF enlargement. This failure to maintain refined RFs and thus preserve high acuity vision in visually deprived adult SC is associated with a loss of GABA and GAD, caused at least in part by a reduction in BDNF-TrkB signaling. In order to explore the postsynaptic mechanism, we examined GABAA receptor expression levels, location, and subunit composition using Western blotting. In addition, we assayed the GABAA receptor anchoring protein gephyrin and expression levels of the chloride transporters KCC2 and NKCC2. To test the alternate hypothesis that RFs enlarge in adulthood as a result of immature postsynaptic NMDA receptors, we examined NR2A/2B ratios and levels of the anchoring protein PSD-95. We found no evidence supporting visual deprivation-related postsynaptic alterations in receptors, chloride transporters, or anchoring proteins in adult hamsters. Thus, we argue that visual deprivation continued past puberty reveals a new form of maladaptive, inhibitory plasticity in which, rather than retaining juvenile features and extending the critical period, continued lack of inhibition in adulthood reopens the critical period, reversing the refinement of receptive fields to the detriment of visual acuity. These results suggest that attempts to increase plasticity in adulthood for purposes of rehabilitation or recovery from injury should consider the possibility of unintended negative consequences.