Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation

Abstract

Visual deprivation during a developmental sensitive period markedly alters visual cortical response properties, but the changes in intracortical circuitry that underlie these effects are poorly understood. Here we use a slice preparation of rat primary visual cortex to show that 2 d of prior visual deprivation early in life increases the excitability of layer 4 circuitry. Slice recordings showed that spontaneous activity of layer 4 star pyramidal neurons increased 25-fold after 2 d of visual deprivation between postnatal days (P) 15 and P17. This effect was mediated by increased net excitatory and decreased net inhibitory synaptic drive. Paired recordings showed that excitatory connections between star pyramidal neurons doubled in amplitude, whereas inhibitory connections decreased or increased depending on the interneuron class. These effects reversed when vision was restored. This dynamic adjustment of the excitation-inhibition balance may allow the networks within layer 4 to maintain stable levels of activity in the face of variable sensory input.

Transcriptomics of critical period of visual cortical plasticity in mice

“…In terms of layer-specific gene expression, we unexpectedly found layer 2/3 to be enriched in pathways and genes involved in cytoskeletal assembly, calcium signaling pathway, MAPK signaling pathway, and long-term potentiation, which suggest that these neurons may be capable of high levels of synaptic plasticity. This result stands in contrast to previous reports indicating that layer 4 is particularly privileged in terms of plasticity (22,23). We found also that layer 5 is enriched for such terms as intermediate filament bundle assembly and regulation of exocytosis, which may be related to the fact that it contains projection neurons that are generally larger and have long-range axons projecting to subcortical targets, necessitating increased production of axonal proteins.…”

Homeostatic Scaling of Vesicular Glutamate and GABA Transporter Expression in Rat Neocortical Circuits

“…Interestingly, VGLUT2 may play such a role in cholinergic motoneurons via a recurrent collateral pathway onto Renshaw inhibitory neurons . Recurrent pyramidal neuron excitatory terminals display differential targeting to subclasses of GABA neurons in the cerebral cortex (DeFelipe, 2002;Melchitzky and Lewis, 2003;Maffei et al, 2004), some of which may provide powerful feedback inhibition onto pyramidal neurons (Reyes et al, 1998;Gupta et al, 2000;McBain and Fisahn, 2001;Markram et al, 2004;Turrigiano and Nelson, 2004). It has been shown in an individual neocortical pyramidal neuron that a 48 h treatment with BIC results in a reduction in quantal amplitude at its cortico-excitatory synapse (feedforward) and an increase in quantal amplitude at its cortico-GABAergic synapse (feedback), which may be attributable, in part, to postsynaptic changes (Rutherford et al, 1997Turrigiano et al, 1998).…”

Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

“…This idea is supported by findings that ODP is enhanced either by increasing GABAergic neurotransmission before the critical period (4) or by reducing GABA signaling after the critical period (5)(6)(7)(8). It has been suggested that, during the critical period, MD itself alters the balance of excitation and feedback inhibition within the visual cortex by depressing the activity of fast-spiking (FS) interneurons (9,10). In support of this idea, ODP is first detectable in the extragranular cortical layers [i.e., 2/3, 5, and 6 (11)], where depression of FS interneuron activity has been reported after brief MD.…”