State Changes Rapidly Modulate Cortical Neuronal Responsiveness

Abstract

The responsiveness of cortical neurons is strongly and rapidly influenced by changes in the level of local network activity. In rodent somatosensory cortex, increases in network activity increase neuronal responsiveness to the intracellular injection of brief conductance stimuli but paradoxically decrease responsiveness to brief whisker deflections. However, whisker stimulation frequently evokes longlasting changes in the level of local circuit activity. The ability of stimuli to successfully evoke prolonged increases in circuit activity is associated with both an increase in the amount of conductance evoked by a whisker stimulus and an increase in action potential responsiveness to whisker stimulation. In addition, brief whisker stimuli presented during periods of high network activity evoke postsynaptic potentials containing a greater proportion of inhibition, consistent with an increased efficiency in the activation of inhibitory mechanisms during the Up state. In contrast, during prolonged and variable whisker stimulation, increased network activity is associated with an increase in overall responsiveness, dynamic range, output gain, and correlation between action potential response and speed of whisker movement. We conclude that stimulus-evoked or spontaneous alterations in cortical state can influence neuronal responsiveness in a complex manner, resulting in large changes in which, and how, sensory stimuli are represented.

Spinal Cord Injury Immediately Changes the State of the Brain

“…However, our results show that the increased cortical responses are directly related to the slower/more silent cortical spontaneous activity, thus offering an additional mechanism to explain immediate changes in cortical responses after deafferentation. In the rat somatosensory system, brief peripheral stimuli evoke larger cortical responses when the cortex is in a silent compared to an active state (Petersen et al, 2003;Sachdev et al, 2004), particularly when the stimuli themselves are able to trigger active states associated with the responses (Hasenstaub et al, 2007;Reig and Sanchez-Vives, 2007). This inverse relation between the level of spontaneous activity and the amplitude of evoked responses is clearly present in our data.…”

“…Note that the multiunit signal we used above to construct the PSTHs of the responses is a point process, whereas the rMUA used here is a time series, representing the compound spiking activity of the local population of neurons around the electrode. The rMUA was chosen because it correlates well with the membrane potential of intracellular recordings and it is thus a good measure of the level of activity in cortical networks (Hasenstaub et al, 2007). The rMUA spectrum was estimated by (1) subtracting the mean to the rMUA, (2) calculating its autocorrelation function, and (3) estimating the power spectral density with Thomson multitaper method.…”

“…The slope ( S) of this inverse correlation between spontaneous activity (in microvolts) and evoked responses (in millivolts) was much steeper for high-intensity stimuli (before transection, S ϭ Ϫ0.110; after transection, S ϭ Ϫ0.168) than for low-intensity stimuli (before transection, S ϭ Ϫ0.056; after transection, S ϭ Ϫ0.067) (Fig. 3C), because low-intensity stimuli are less likely to trigger active states associated with the response than high-intensity stimuli (Hasenstaub et al, 2007;Reig and Sanchez-Vives, 2007). This could explain why the increased forepaw responses were specifically observed with high-intensity stimuli: after the deafferentation imposed by thoracic transection of the spinal cord, forepaw stimuli are more likely to occur when the cortex is more silent, but only high-intensity stimuli are able to consistently trigger active states, and thus to evoke larger cortical responses.…”

Sensory experience modifies spontaneous state dynamics in a large-scale barrel cortical model

“…For example, cortical neuronal responses to repeated application of the same stimulus have a high degree of trial-to-trial variability (Arieli et al 1996, Azouz & Gray 1999, Fox et al 2007, much of which is due to spontaneous membrane potential fluctuations (reflecting the spontaneous activity of the network incipient to a neuron). Furthermore, the spontaneous fluctuations in the membrane potential, the UP and DOWN states, were shown to affect the responsiveness of cortical neurons to whisker stimulation (Hasenstaub et al 2007).…”

Interaction of slow cortical rhythm with somatosensory information processing in urethane-anesthetized rats

“…Active (depolarized) states were first referred as UP states, while silent (hyperpolarized) epochs as DOWN states in the basal ganglia (Wilson & Kawaguchi, 1996). Strong correlation was found between SCR states and membrane potential fluctuations of striatal medium spiny neurons (Kasanetz et al, 2006), hippocampal interneurons (Hahn et al, 2006) and cortical neurons (Steriade et al, 1993a;Haider et al, 2006;Hasenstaub et al, 2007;Haider et al, 2007). SCR was declared to be of cortical origin as thalamic ablations did not abolish cortical active and silent states (Steriade et al, 1993b) and cortical ablations prevented active states from occurring in the striatum and thalamus (Nita et al, 2003;Steriade et al, 1993b).…”