Plasticity between Neuronal Pairs in Layer 4 of Visual Cortex Varies with Synapse State

In neocortex, the induction and expression of long-term potentiation (LTP) and long-term depression (LTD) vary depending on cortical area and laminae of presynaptic and postsynaptic neurons. Layer 4 (L4) is the initial site of sensory afference in barrel cortex and primary visual cortex (V1) in which excitatory inputs from thalamus, L6, and neighboring L4 cells are integrated. However, little is known about plasticity within L4. We studied plasticity at excitatory synaptic connections between pairs and triplets of interconnected L4 neurons in guinea pig V1 using a fixed delay pairing protocol. Plasticity outcomes were heterogeneous, with some connections undergoing LTP (n = 7 of 42), some LTD (n = 19 of 42), and some not changing (n = 16 of 42). Although quantal analysis revealed both presynaptic and postsynaptic plasticity expression components, reduction in quantal size (a postsynaptic property) contributing to LTD was ubiquitous, whereas in some cell pairs, this change was overridden by an increase in the probability of neurotransmitter release (a presynaptic property) resulting in LTP. These changes depended on the initial reliability of the connections: highly reliable connections depressed with contributions from presynaptic and postsynaptic effects, and unreliable connections potentiated as a result of the predominance of presynaptic enhancement. Interestingly, very strong, reliable pairs of connected cells showed little plasticity. Pairs of connected cells with a common presynaptic or postsynaptic L4 cell behaved independently, undergoing plasticity of different or opposite signs. Release probability of a connection with initial 100% failure rate was enhanced after pairing, potentially avoiding silencing of the presynaptic terminal and maintaining L4-L4 synapses in a broader dynamic range.