How the mechanisms of long-term synaptic potentiation and depression serve experience-dependent plasticity in primary visual cortex

Abstract

Donald Hebb chose visual learning in primary visual cortex (V1) of the rodent to exemplify his theories of how the brain stores information through long-lasting homosynaptic plasticity. Here, we revisit V1 to consider roles for bidirectional ‘Hebbian’ plasticity in the modification of vision through experience. First, we discuss the consequences of monocular deprivation (MD) in the mouse, which have been studied by many laboratories over many years, and the evidence that synaptic depression of excitatory input from the thalamus is a primary contributor to the loss of visual cortical responsiveness to stimuli viewed through the deprived eye. Second, we describe a less studied, but no less interesting form of plasticity in the visual cortex known as stimulus-selective response potentiation (SRP). SRP results in increases in the response of V1 to a visual stimulus through repeated viewing and bears all the hallmarks of perceptual learning. We describe evidence implicating an important role for potentiation of thalamo-cortical synapses in SRP. In addition, we present new data indicating that there are some features of this form of plasticity that cannot be fully accounted for by such feed-forward Hebbian plasticity, suggesting contributions from intra-cortical circuit components.

Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling

“…That said, experiments in rodents [87] have isolated the binocular lateral geniculate nucleus inputs to layer 4 cells and have shown that the classic properties of ocular dominance plasticity exist at these synapses [88][89][90], which thus form the most straightforward testbed for understanding the synaptic mechanisms that underlie a behaviourally relevant form of plasticity. There seems to be general agreement that the initial weakening of the deprived eye depends on homosynaptic LTD [91]. Several types of experiments have demonstrated that biochemical alterations that block LTD in slice experiments can block the downregulation of the V1 response to the deprived eye.…”

Experience-Dependent Synaptic Plasticity in V1 Occurs without Microglial CX3CR1

“…Therefore, we next investigated how 3 d of MD affects thalamocortical synapse size and density using quantitative immuno-EM. We used the vesicular glutamate transporter (VGluT2) antibody to specifically label thalamocortical terminals in the mouse (Nahmani and Erisir, 2005;Coleman et al, 2010). This approach allows separate analysis of presynaptic input that originates from the LGN and other (mostly intracortical) sources (Fig.…”

“…It has been established that functional deprived-eye depression in layer 4 (L4) is mediated by NMDA receptor (NMDAR)-dependent AMPA receptor (AMPAR) internalization (for review, see Cooke and Bear, 2014). Additionally, there are well known anatomical changes in geniculocortical axons and synapses after MD (Hubel et al, 1977;Shatz and Stryker, 1978;Friedlander et al, 1991;Antonini and Stryker, 1993;Antonini et al, 1999). Quantitative immunoelectron microscopy (immuno-EM) in the mouse binocular visual cortex demonstrates that structural effects of MD can occur as rapidly as the functional, electrophysiologically measured effects (Coleman et al, 2010).…”

“…Additionally, there are well known anatomical changes in geniculocortical axons and synapses after MD (Hubel et al, 1977;Shatz and Stryker, 1978;Friedlander et al, 1991;Antonini and Stryker, 1993;Antonini et al, 1999). Quantitative immunoelectron microscopy (immuno-EM) in the mouse binocular visual cortex demonstrates that structural effects of MD can occur as rapidly as the functional, electrophysiologically measured effects (Coleman et al, 2010). However, the mechanisms that couple and coordinate functional and structural plasticity are largely unidentified.…”

A metaplasticity view of the interaction between homeostatic and Hebbian plasticity

“…Other research has detailed further dynamics of ODP, showing that in addition to Hebbian deprived-eye response depression, prolonged MD leads to a second Hebbian phase of potentiation in responsiveness to the non-deprived eye [23,33]. For a more comprehensive review on Hebbian plasticity in the primary visual cortex, please see Cooke & Bear [39].…”