scholarly journals Visual experience prevents dysregulation of GABAB receptor-dependent short-term depression in adult superior colliculus

2015 ◽  
Vol 113 (7) ◽  
pp. 2049-2061 ◽  
Author(s):  
Timothy S. Balmer ◽  
Sarah L. Pallas

Progressive loss of plasticity during development prevents refined circuits from regressing to an immature state and is thought to depend on maturation of GABAergic inhibition. For example, a gradual reduction in size of visual receptive fields (RFs) occurs in the superior colliculus (SC) during development. Maintenance of the refined state throughout adulthood requires early light exposure. Here we investigate the potential role of changes in long- or short-term plasticity in experience-dependent maintenance of refined RFs. Using an acute SC slice preparation, we found that long-term plasticity was not affected by visual deprivation, indicating that it does not underlie deprivation-induced RF enlargement. In contrast, visual deprivation altered short-term plasticity in an unexpected way. Specifically, GABAB receptor (GABABR)-mediated paired pulse depression was increased in slices from dark-reared animals. This increase was mimicked by GABAAR blockade in slices from normally reared animals, suggesting that experience-dependent maintenance of GABAAR function prevents an increase in probability of neurotransmitter release. GABABR-mediated short-term depression in response to strong stimulation (such as occurs during vision) was reduced in slices from dark-reared animals. This change was mimicked in slices from normal animals by reducing GABA release. These results are consistent with the hypothesis that early visual experience maintains GABAergic inhibition and prevents later deprivation-induced alterations of short-term depression in SC. Identifying how plasticity is restricted in mature circuits could guide therapies to enhance recovery of function in adults.

2005 ◽  
Vol 94 (3) ◽  
pp. 1962-1970 ◽  
Author(s):  
M. M. Carrasco ◽  
K. A. Razak ◽  
S. L. Pallas

Sensory deprivation is thought to have an adverse effect on visual development and to prolong the critical period for plasticity. Once the animal reaches adulthood, however, synaptic connectivity is understood to be largely stable. We reported previously that N-methyl-d-aspartate (NMDA) receptor blockade in the superior colliculus of the Syrian hamster prevents refinement of receptive fields (RFs) in normal or compressed retinotopic projections, resulting in target neurons with enlarged RFs but normal stimulus tuning. Here we asked whether visually driven activity is necessary for refinement or maintenance of retinotopic maps or if spontaneous activity is sufficient. Animals were deprived of light either in adulthood only or from birth until the time of recording. We found that dark rearing from birth to 2 mo of age had no effect on the timing and extent of RF refinement as assessed with single unit extracellular recordings. Visual deprivation in adulthood also had no effect. Continuous dark rearing from birth into adulthood, however, resulted in a progressive loss of refinement, resulting in enlarged, asymmetric receptive fields and altered surround suppression in adulthood. Thus unlike in visual cortex, early visually driven activity is not necessary for refinement of receptive fields during development, but is required to maintain refined visual projections in adulthood. Because the map can refine normally in the dark, these results argue against a deprivation-induced delay in critical period closure, and suggest instead that early visual deprivation leaves target neurons more vulnerable to deprivation that continues after refinement.


2020 ◽  
Author(s):  
Aniello Lombardi ◽  
Peter Jedlicka ◽  
Heiko J. Luhmann ◽  
Werner Kilb

AbstractThe impact of GABAergic transmission on neuronal excitability depends on the Cl−-gradient across membranes. However, the Cl−-fluxes through GABAA receptors alter the intracellular Cl− concentration ([Cl−]i) and in turn attenuate GABAergic responses, a process termed ionic plasticity. Recently it has been shown that coincident glutamatergic inputs significantly affect ionic plasticity. Yet how the [Cl−]i changes depend on the properties of glutamatergic inputs and their spatiotemporal relation to GABAergic stimuli is unknown. To investigate this issue, we used compartmental biophysical models of Cl− dynamics simulating either a simple ball-and-stick topology or a reconstructed immature CA3 neuron. These computational experiments demonstrated that glutamatergic co-stimulation enhances GABA receptor-mediated Cl− influx at low and attenuates or reverses the Cl− efflux at high initial [Cl−]i. The size of glutamatergic influence on GABAergic Cl−-fluxes depends on the conductance, decay kinetics, and localization of glutamatergic inputs. Surprisingly, the glutamatergic shift in GABAergic Cl−-fluxes is invariant to latencies between GABAergic and glutamatergic inputs over a substantial interval. In agreement with experimental data, simulations in a reconstructed CA3 pyramidal neuron with physiological patterns of correlated activity revealed that coincident glutamatergic synaptic inputs contribute significantly to the activity-dependent [Cl−]i changes. Whereas the influence of spatial correlation between distributed glutamatergic and GABAergic inputs was negligible, their temporal correlation played a significant role. In summary, our results demonstrate that glutamatergic co-stimulation had a substantial impact on ionic plasticity of GABAergic responses, enhancing the destabilization of GABAergic inhibition in the mature nervous systems, but suppressing GABAergic [Cl−]i changes in the immature brain. Therefore, glutamatergic shift in GABAergic Cl−-fluxes should be considered as a relevant factor of short term plasticity.Author SummaryInformation processing in the brain requires that excitation and inhibition are balanced. The main inhibitory neurotransmitter in the brain is gamma-amino-butyric acid (GABA). GABA actions depend on the Cl−-gradient, but activation of ionotropic GABA receptors causes Cl−-fluxes and thus reduces GABAergic inhibition. Here, we investigated how a coincident membrane depolarization by excitatory, glutamatergic synapses influences GABA-induced Cl−-fluxes using a biophysical compartmental model of Cl− dynamics, simulating either simple or realistic neuron topologies. We demonstrate that glutamatergic co-stimulation directly affects GABA-induced Cl−-fluxes, with the size of glutamatergic effects depending on the conductance, the decay kinetics, and localization of glutamatergic inputs. We also show that the glutamatergic shift in GABAergic Cl−-fluxes is surprisingly stable over a substantial range of latencies between glutamatergic and GABAergic inputs. We conclude from these results that glutamatergic co-stimulation alters GABAergic Cl−-fluxes and in turn affects the strength of GABAergic inhibition. These coincidence-dependent ionic changes should be considered as a relevant factor of short term plasticity in the CNS.


2013 ◽  
Vol 109 (2) ◽  
pp. 464-474 ◽  
Author(s):  
Liping Yu ◽  
Benjamin A. Rowland ◽  
Jinghong Xu ◽  
Barry E. Stein

Multisensory superior colliculus neurons in cats were found to retain substantial plasticity to short-term, site-specific experience with cross-modal stimuli well into adulthood. Following cross-modal exposure trials, these neurons substantially increased their sensitivity to the cross-modal stimulus configuration as well as to its individual component stimuli. In many cases, the exposure experience also revealed a previously ineffective or “silent” input channel, rendering it overtly responsive. These experience-induced changes required relatively few exposure trials and could be retained for more than 1 h. However, their induction was generally restricted to experience with cross-modal stimuli. Only rarely were they induced by exposure to a modality-specific stimulus and were never induced by stimulating a previously ineffective input channel. This short-term plasticity likely provides substantial benefits to the organism in dealing with ongoing and sequential events that take place at a given location in space and may reflect the ability of multisensory superior colliculus neurons to rapidly alter their response properties to accommodate to changes in environmental challenges and event probabilities.


2006 ◽  
Vol 23 (6) ◽  
pp. 845-852 ◽  
Author(s):  
MARÍA MAGDALENA CARRASCO ◽  
SARAH L. PALLAS

The role of sensory experience in the development and plasticity of the visual system has been widely studied. It has generally been reported that once animals reach adulthood, experience-dependent visual plasticity is reduced. We have found that visual experience is not needed for the refinement of receptive fields (RFs) in the superior colliculus (SC) but instead is necessary to maintain them in adulthood (Carrasco et al., 2005). Without light exposure, RFs in SC of hamsters refine by postnatal day 60 as usual but then enlarge, presumably reducing visual acuity. In this study we examine whether a brief period of light exposure during early postnatal development would be sufficient to prevent RF enlargement in adulthood, and whether prolonged light exposure in adulthood could reverse the deprivation-induced increase in RF size. We found that an early postnatal period of at least 30 days of visual experience was sufficient to maintain refined RFs in the adult SC. Prolonged visual experience in adulthood could not reverse the RF enlargement resulting from long-term dark rearing, reflecting a loss of plasticity at this age. Our results suggest that, unlike in visual cortex, dark rearing does not indefinitely extend the critical period of plasticity in SC. Rather, there is a limited time window when early experience can protect RFs from the detrimental effects of visual deprivation in adulthood. These results contribute to understanding adult brain plasticity and argue for the importance of early visual experience in protecting the adult visual system.


1997 ◽  
Vol 101 (1) ◽  
pp. 229-239 ◽  
Author(s):  
Jose C. Ramalho ◽  
Thos L. Pons ◽  
Henri W. Groeneveld ◽  
M. Antonieta Nunes

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