Bidirectional Plasticity of Intrinsic Excitability Controls Sensory Inputs Efficiency in Layer 5 Barrel Cortex Neuronsin Vivo

Abstract

Responsiveness of cortical neurons to sensory inputs can be altered by experience and learning. While synaptic plasticity is generally proposed as the underlying cellular mechanism, possible contributions of activity-dependent changes in intrinsic excitability remain poorly investigated. Here, we show that periods of rhythmic firing in rat barrel cortex layer 5 pyramidal neurons can trigger a long-lasting increase or decrease in their membrane excitability in vivo. Potentiation of cortical excitability consisted of an increased firing in response to intracellular stimulation and a reduction in threshold current for spike initiation. Conversely, depression of cortical excitability was evidenced by an augmented firing threshold leading to a reduced current-evoked spiking. The direction of plasticity depended on the baseline level of spontaneous firing rate and cell excitability. We also found that changes in intrinsic excitability were accompanied by corresponding modifications in the effectiveness of sensory inputs. Potentiation and depression of cortical neuron excitability resulted, respectively, in an increased or decreased firing probability on whisker-evoked synaptic responses, without modifications in the synaptic strength itself. These data suggest that bidirectional intrinsic plasticity could play an important role in experience-dependent refinement of sensory cortical networks.

Toward a Neurocentric View of Learning

“…Intrinsic potentiation occurred about twice as often as depression (Paz et at., 2009). Similarly, repeated current injection caused intrinsic potentiation (18/30) or depression (12/30) in layer 5 pyramidal neurons of the barrel cortex of anesthetized rats (Mahon and Charpier, 2012; for example traces from layer 2/3 barrel cortex neurons, see Fig. 2).…”

Impaired neuronal operation through aberrant intrinsic plasticity in epilepsy

“…We applied linear regressions to individual f/I curves and collected the neuronal gain, defined as the slope of the f/I curve 56,57 . The rheobase was measured as the minimal current amplitude necessary to evoke an action potential.…”

“…Intrinsic plasticity can also be involved in homeostatic mechanisms to normalize neuronal firing as shown in vitro and in vivo 57,73,74 . Different types of currents have been reported to contribute to intrinsic plasticity including I NaT 75-77 , I h 78 and Kv1 channel activity 79 affecting the spike threshold.…”

Contextual fear conditioning depresses infralimbic excitability

“…Relatively brief stimulation of neurons in brain slices or in vivo is sufficient to induce a long-lasting plasticity of intrinsic excitability (Daoudal et al, 2002; Mahon and Charpier, 2012). Both the dorsal (dHPC) and ventral (vHPC) hippocampus innervate IL and are critical for contextual fear (Cenquizca and Swanson, 2007; Hoover and Vertes, 2007; Hunsaker and Kesner, 2008; Fanselow and Dong, 2010; Liu et al, 2012; Maren et al, 2013).…”