Thalamic inhibition regulates critical-period plasticity in visual cortex and thalamus

Abstract

During critical periods of development, experience shapes cortical circuits, resulting in the acquisition of functions used throughout life. The classic example of critical-period plasticity is ocular dominance (OD) plasticity, which optimizes binocular vision but can reduce the responsiveness of the primary visual cortex (V1) to an eye providing low-grade visual input. The onset of the critical period of OD plasticity involves the maturation of inhibitory synapses within V1, specifically those containing the GABA receptor α1 subunit. Here we show that thalamic relay neurons in mouse dorsolateral geniculate nucleus (dLGN) also undergo OD plasticity. This process depends on thalamic α1-containing synapses and is required for consolidation of the OD shift in V1 during long-term deprivation. Our findings demonstrate that thalamic inhibitory circuits play a central role in the regulation of the critical period. This has far-reaching consequences for the interpretation of studies investigating the molecular and cellular mechanisms regulating critical periods of brain development.

Synaptic plasticity onto inhibitory neurons as a mechanism for ocular dominance plasticity

“…We only considered plasticity in connections from layer IV to layer II/III and within layer II/III. Therefore, we did not take into account experimentally observed OD shifts in the thalamic relay neurons [Sommeijer et al, 2017, Jaepel et al, 2017 and layer IV neurons [Gordon and Stryker, 1996]. Since these areas are upstream of layer II/III, a naive explanation could be that the shift in layer II/III is fully accounted for by the shift in the inputs to this layer.…”

“…A well studied example is the critical period for ocular dominance (OD) in primary visual cortex (V1). In the visual pathway, inputs from both eyes usually converge onto the same neuron for the first time in V1, although a fraction of thalamic neurons already exhibits binocularity in mice [Jaepel et al, 2017, Sommeijer et al, 2017, Jeon and Kuhlman, 2017. The extent to which a neuron's visually-evoked activity is dominated by one of the eyes is called ocular dominance (OD) and is often quantified by the ocular dominance index (ODI).…”

Critical-Period Visual Deprivation Disrupts Binocular Integration but Spares Spatial Acuity in the Geniculocortical Pathway

“…A functional study (Jaepel et al, 2017) showed that ocular dominance of thalamic axons in V1 can be altered by short-term (6-8 days) MD under plasticity-enhancing conditions in adult mice but the effect was found to be transient. Another study (Sommeijer et al, 2017) reported that 7 days of MD during the critical period can lead to an ocular dominance shift in dLGN neurons. However, these studies did not address whether long-term MD during the critical period, a manipulation that has been shown to have a long-lasting impact on the animal's visual acuity (Davis et al, 2015;Prusky and Douglas, 2003;Stephany et al, 2014), can lead to persistent changes in dLGN visual properties, including binocular integration.…”

“…A growing body of recent evidence indicates that significant binocular processing occurs in dLGN in mice (Howarth et al, 2014;Jaepel et al, 2017;Sommeijer et al, 2017) and marmosets (Zeater et al, 2015). A retrograde tracing study (Rompani et al, 2017) demonstrated that single dLGN neurons receive direct retinal inputs from both eyes, providing an anatomical substrate for binocular integration in the mouse dLGN.…”

Cortical inactivation does not block response enhancement in the superior colliculus

“…Little is known about the effect of visual training at the subcortical level. A study carried out on the rat's dorsal lateral geniculate nucleus (dLGN), the primary recipient of visual information, suggests that the response properties of thalamic neurons are subject to experience-dependent long-term plasticity [21,22]. Similarly, in the superior colliculus (SC), the second major target of retinal input, repetitive exposure to dimming stimuli effectively induced the LTP of developing retinotectal synapses in Xenopus tadpole [23].…”