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UP states protect ongoing cortical activity from thalamic inputs.

Watson BO, MacLean JN, Yuste R - PLoS ONE (2008)

Bottom Line: To examine how thalamic inputs interact with ongoing cortical UP state activity, we used calcium imaging and targeted whole-cell recordings of activated neurons in thalamocortical slices of mouse somatosensory cortex.Both thalamocortical and corticocortical PSPs were significantly reduced and neuronal input resistance was significantly decreased during cortical UP states -- mechanistically consistent with UP state insensitivity.Our results demonstrate that cortical dynamics during UP states are insensitive to thalamic inputs.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Department of Biological Sciences, Columbia University, New York, NY, USA. bow4@columbia.edu

ABSTRACT
Cortical neurons in vitro and in vivo fluctuate spontaneously between two stable membrane potentials: a depolarized UP state and a hyperpolarized DOWN state. UP states temporally correspond with multineuronal firing sequences which may be important for information processing. To examine how thalamic inputs interact with ongoing cortical UP state activity, we used calcium imaging and targeted whole-cell recordings of activated neurons in thalamocortical slices of mouse somatosensory cortex. Whereas thalamic stimulation during DOWN states generated multineuronal, synchronized UP states, identical stimulation during UP states had no effect on the subthreshold membrane dynamics of the vast majority of cells or on ongoing multineuronal temporal patterns. Both thalamocortical and corticocortical PSPs were significantly reduced and neuronal input resistance was significantly decreased during cortical UP states -- mechanistically consistent with UP state insensitivity. Our results demonstrate that cortical dynamics during UP states are insensitive to thalamic inputs.

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Thalamic stimulation does not perturb membrane potential during UP states.(a) Simultaneous whole-cell recordings in two neurons reveal spontaneously arising UP states. Boxed areas shown at higher temporal resolution below. (b) Simultaneous whole cell recordings of the same neurons reveal UP states following thalamic stimulation that was manually triggered during a cortical DOWN state. (c) Simultaneous whole cell recordings of the same neurons during a spontaneous UP state with an automatically-triggered thalamic stimulation. Arrow indicates time of thalamic activation. Boxed area around the stimulus itself is shown at higher resolution below. There is no observable change in the UP state as a result of the thalamic stimulation occurring during the ongoing UP state. (d) Quantification of population spike rates during spontaneous UP states versus UP states resulting from thalamic stimulation during the DOWN state versus spontaneous UP states with impinging thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. None of the measured spike rate means of different types of UP states were significantly different (p>0.10 by bootstrap resampling). The third bar represents a linear summation between spiking during spontaneous UP states and that triggered by thalamic stimulation during the DOWN state. The value calculated in this summation differs significantly from all measured values (by bootstrap resampling, p<.001, indicated by *), including the value of spontaneous UP states with interacting added thalamic stimulation. (e1) Similar recordings of a different pair of neurons during a thalamically stimulated UP state with a subsequent thalamic stimulation occurring during the UP state. Arrows indicate times of thalamic activation. Similar to ongoing spontaneous UP states, there is no observable change in membrane potential as a result of the thalamic stimulation. (f) Quantification of population spike rates during thalamically stimulated UP states versus thalamically stimulated UP states interacting with thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. A second thalamic stimulation during an UP state did not increase spiking during UP states (p>0.10). The value calculated in this summation differs significantly from measured values (by bootstrap resampling, p<.001, indicated by *), including the value of stimulated UP states with interacting added thalamic stimulation.
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pone-0003971-g005: Thalamic stimulation does not perturb membrane potential during UP states.(a) Simultaneous whole-cell recordings in two neurons reveal spontaneously arising UP states. Boxed areas shown at higher temporal resolution below. (b) Simultaneous whole cell recordings of the same neurons reveal UP states following thalamic stimulation that was manually triggered during a cortical DOWN state. (c) Simultaneous whole cell recordings of the same neurons during a spontaneous UP state with an automatically-triggered thalamic stimulation. Arrow indicates time of thalamic activation. Boxed area around the stimulus itself is shown at higher resolution below. There is no observable change in the UP state as a result of the thalamic stimulation occurring during the ongoing UP state. (d) Quantification of population spike rates during spontaneous UP states versus UP states resulting from thalamic stimulation during the DOWN state versus spontaneous UP states with impinging thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. None of the measured spike rate means of different types of UP states were significantly different (p>0.10 by bootstrap resampling). The third bar represents a linear summation between spiking during spontaneous UP states and that triggered by thalamic stimulation during the DOWN state. The value calculated in this summation differs significantly from all measured values (by bootstrap resampling, p<.001, indicated by *), including the value of spontaneous UP states with interacting added thalamic stimulation. (e1) Similar recordings of a different pair of neurons during a thalamically stimulated UP state with a subsequent thalamic stimulation occurring during the UP state. Arrows indicate times of thalamic activation. Similar to ongoing spontaneous UP states, there is no observable change in membrane potential as a result of the thalamic stimulation. (f) Quantification of population spike rates during thalamically stimulated UP states versus thalamically stimulated UP states interacting with thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. A second thalamic stimulation during an UP state did not increase spiking during UP states (p>0.10). The value calculated in this summation differs significantly from measured values (by bootstrap resampling, p<.001, indicated by *), including the value of stimulated UP states with interacting added thalamic stimulation.

Mentions: While we were able to demonstrate that there was no effect of impinging thalamic stimulation on the population spiking patterns during UP states, we wanted to use a more sensitive method than calcium imaging to assess the effects on single neurons. We therefore patch clamped 57 neurons and recorded their firing in UP states while we stimulated the thalamus (Figure 5).


UP states protect ongoing cortical activity from thalamic inputs.

Watson BO, MacLean JN, Yuste R - PLoS ONE (2008)

Thalamic stimulation does not perturb membrane potential during UP states.(a) Simultaneous whole-cell recordings in two neurons reveal spontaneously arising UP states. Boxed areas shown at higher temporal resolution below. (b) Simultaneous whole cell recordings of the same neurons reveal UP states following thalamic stimulation that was manually triggered during a cortical DOWN state. (c) Simultaneous whole cell recordings of the same neurons during a spontaneous UP state with an automatically-triggered thalamic stimulation. Arrow indicates time of thalamic activation. Boxed area around the stimulus itself is shown at higher resolution below. There is no observable change in the UP state as a result of the thalamic stimulation occurring during the ongoing UP state. (d) Quantification of population spike rates during spontaneous UP states versus UP states resulting from thalamic stimulation during the DOWN state versus spontaneous UP states with impinging thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. None of the measured spike rate means of different types of UP states were significantly different (p>0.10 by bootstrap resampling). The third bar represents a linear summation between spiking during spontaneous UP states and that triggered by thalamic stimulation during the DOWN state. The value calculated in this summation differs significantly from all measured values (by bootstrap resampling, p<.001, indicated by *), including the value of spontaneous UP states with interacting added thalamic stimulation. (e1) Similar recordings of a different pair of neurons during a thalamically stimulated UP state with a subsequent thalamic stimulation occurring during the UP state. Arrows indicate times of thalamic activation. Similar to ongoing spontaneous UP states, there is no observable change in membrane potential as a result of the thalamic stimulation. (f) Quantification of population spike rates during thalamically stimulated UP states versus thalamically stimulated UP states interacting with thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. A second thalamic stimulation during an UP state did not increase spiking during UP states (p>0.10). The value calculated in this summation differs significantly from measured values (by bootstrap resampling, p<.001, indicated by *), including the value of stimulated UP states with interacting added thalamic stimulation.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2597736&req=5

pone-0003971-g005: Thalamic stimulation does not perturb membrane potential during UP states.(a) Simultaneous whole-cell recordings in two neurons reveal spontaneously arising UP states. Boxed areas shown at higher temporal resolution below. (b) Simultaneous whole cell recordings of the same neurons reveal UP states following thalamic stimulation that was manually triggered during a cortical DOWN state. (c) Simultaneous whole cell recordings of the same neurons during a spontaneous UP state with an automatically-triggered thalamic stimulation. Arrow indicates time of thalamic activation. Boxed area around the stimulus itself is shown at higher resolution below. There is no observable change in the UP state as a result of the thalamic stimulation occurring during the ongoing UP state. (d) Quantification of population spike rates during spontaneous UP states versus UP states resulting from thalamic stimulation during the DOWN state versus spontaneous UP states with impinging thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. None of the measured spike rate means of different types of UP states were significantly different (p>0.10 by bootstrap resampling). The third bar represents a linear summation between spiking during spontaneous UP states and that triggered by thalamic stimulation during the DOWN state. The value calculated in this summation differs significantly from all measured values (by bootstrap resampling, p<.001, indicated by *), including the value of spontaneous UP states with interacting added thalamic stimulation. (e1) Similar recordings of a different pair of neurons during a thalamically stimulated UP state with a subsequent thalamic stimulation occurring during the UP state. Arrows indicate times of thalamic activation. Similar to ongoing spontaneous UP states, there is no observable change in membrane potential as a result of the thalamic stimulation. (f) Quantification of population spike rates during thalamically stimulated UP states versus thalamically stimulated UP states interacting with thalamic input. Bars represent means of mean spike rates for each cell, and error bars represent standard error of the mean. A second thalamic stimulation during an UP state did not increase spiking during UP states (p>0.10). The value calculated in this summation differs significantly from measured values (by bootstrap resampling, p<.001, indicated by *), including the value of stimulated UP states with interacting added thalamic stimulation.
Mentions: While we were able to demonstrate that there was no effect of impinging thalamic stimulation on the population spiking patterns during UP states, we wanted to use a more sensitive method than calcium imaging to assess the effects on single neurons. We therefore patch clamped 57 neurons and recorded their firing in UP states while we stimulated the thalamus (Figure 5).

Bottom Line: To examine how thalamic inputs interact with ongoing cortical UP state activity, we used calcium imaging and targeted whole-cell recordings of activated neurons in thalamocortical slices of mouse somatosensory cortex.Both thalamocortical and corticocortical PSPs were significantly reduced and neuronal input resistance was significantly decreased during cortical UP states -- mechanistically consistent with UP state insensitivity.Our results demonstrate that cortical dynamics during UP states are insensitive to thalamic inputs.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Department of Biological Sciences, Columbia University, New York, NY, USA. bow4@columbia.edu

ABSTRACT
Cortical neurons in vitro and in vivo fluctuate spontaneously between two stable membrane potentials: a depolarized UP state and a hyperpolarized DOWN state. UP states temporally correspond with multineuronal firing sequences which may be important for information processing. To examine how thalamic inputs interact with ongoing cortical UP state activity, we used calcium imaging and targeted whole-cell recordings of activated neurons in thalamocortical slices of mouse somatosensory cortex. Whereas thalamic stimulation during DOWN states generated multineuronal, synchronized UP states, identical stimulation during UP states had no effect on the subthreshold membrane dynamics of the vast majority of cells or on ongoing multineuronal temporal patterns. Both thalamocortical and corticocortical PSPs were significantly reduced and neuronal input resistance was significantly decreased during cortical UP states -- mechanistically consistent with UP state insensitivity. Our results demonstrate that cortical dynamics during UP states are insensitive to thalamic inputs.

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