Prolonged Disynaptic Inhibition in the Cortex Mediated by Slow, Non-α7 Nicotinic Excitation of a Specific Subset of Cortical Interneurons

Arroyo, Sergio; Bennett, Corbett; Aziz, David; Brown, Solange P.; Hestrin, Shaul

doi:10.1523/jneurosci.0115-12.2012

Cited by 137 publications

(192 citation statements)

References 33 publications

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“…These endeavors will help us understand how information about attention, learning, motivational salience, and arousal converge and interact in this underexplored nexus of the brain. Ultimately, this information will be crucial in designing specific treatments for disorders that affect BF function, such as coma (Brown et al, 2010), sleep disorders (Brown et al, 2012), dementia (Cummings and Benson, 1984), Alzheimer's disease (Whitehouse et al, 1982;Grothe et al, 2012), and normal cognitive aging (Gallagher and Colombo, 1995).…”

Section: Discussionmentioning

confidence: 99%

“…Cholinergic input to the cortex has long been considered to act as a global activating system (Buzsaki et al, 1988;Metherate et al, 1992;Brown et al, 2012;Pinto et al, 2013), but until recently, there were no direct measurements of cholinergic signaling and cortical state changes on rapid timescales with behavioral relevance in awake mice.…”

Section: Bf Cholinergic Signaling Controls Cortical States During Whimentioning

confidence: 99%

“…The basal forebrain (BF) contains multiple major ascending arousal systems that promote wakefulness, awareness, and cortical low-voltage fast activity (Moruzzi and Magoun, 1949;Semba, 2000;Jones, , 2004Brown et al, 2012;. The BF has also long been implicated in cognitive functions, including attention, learning, and motivational salience (DeLong, 1971;Richardson and DeLong, 1990;Wilson and Rolls, 1990a;Voytko et al, 1994;Voytko, 1996;Lin and Nicolelis, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition

et al. 2015

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The basal forebrain (BF) houses major ascending projections to the entire neocortex that have long been implicated in arousal, learning, and attention. The disruption of the BF has been linked with major neurological disorders, such as coma and Alzheimer's disease, as well as in normal cognitive aging. Although it is best known for its cholinergic neurons, the BF is in fact an anatomically and neurochemically complex structure. Recent studies using transgenic mouse lines to target specific BF cell types have led to a renaissance in the study of the BF and are beginning to yield new insights about cell-type-specific circuit mechanisms during behavior. These approaches enable us to determine the behavioral conditions under which cholinergic and noncholinergic BF neurons are activated and how they control cortical processing to influence behavior. Here we discuss recent advances that have expanded our knowledge about this poorly understood brain region and laid the foundation for future cell-type-specific manipulations to modulate arousal, attention, and cortical plasticity in neurological disorders.

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Section: Discussionmentioning

confidence: 99%

Section: Bf Cholinergic Signaling Controls Cortical States During Whimentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition

et al. 2015

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“…Cholinergic axons, which predominately originate from the basal forebrain in rodents, widely innervate all areas and layers of the neocortex (Mechawar et al, 2000;Arroyo et al, 2012;Kalmbach et al, 2012), with a particularly high density in neocortical layer 1 (Mechawar et al, 2000). Layer 1 is a unique neocortical layer that is devoid of excitatory neurons, but contains a rich plexus of axons, the apical dendrites of pyramidal neurons, and a relatively low density of GABAergic interneurons (Winer and Larue, 1989;Prieto et al, 1994).…”

Section: Introductionmentioning

confidence: 99%

“…Layer 1 is a unique neocortical layer that is devoid of excitatory neurons, but contains a rich plexus of axons, the apical dendrites of pyramidal neurons, and a relatively low density of GABAergic interneurons (Winer and Larue, 1989;Prieto et al, 1994). Layer 1 interneurons form cell-class specific circuits in the neocortex (Chu et al, 2003;Letzkus et al, 2011;Wozny and Williams, 2011;Arroyo et al, 2012;Jiang et al, 2013). One class of layer 1 interneurons, neurogliaform cells (NGFCs), provide a direct source of apical dendritic inhibition to layer 2/3 and layer 5 pyramidal neurons by the activation of GABA B receptors (Tamás et al, 2003;Oláh et al, 2009;Wozny and Williams, 2011;Palmer et al, 2012;Jiang et al, 2013), whereas other classes of layer 1 interneurons predominately disinhibit pyramidal neurons through disynaptic circuits (Christophe et al, 2002;Letzkus et al, 2011;Arroyo et al, 2012;Jiang et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Activity-Dependent Modulation of Layer 1 Inhibitory Neocortical Circuits by Acetylcholine

2014

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Layer 1 neocortical GABAergic interneurons control the excitability of pyramidal neurons through cell-class-specific direct inhibitory and disynaptic disinhibitory circuitry. The engagement of layer 1 inhibitory circuits during behavior is powerfully controlled by the cholinergic neuromodulatory system. Here we report that acetylcholine (ACh) influences the excitability of layer 1 interneurons in a cell-class and activity-dependent manner. Whole-cell recordings from identified layer 1 interneurons of the rat somatosensory neocortex revealed that brief perisomatic application of ACh excited both neurogliaform cells (NGFCs) and classical-accommodating cells (c-ACs) at rest by the activation of nicotinic receptors. In contrast, under active, action potential firing states, ACh excited c-ACs, but inhibited NGFCs through muscarinic receptor-mediated, IP 3 receptor-dependent elevations of intracellular calcium that gated surface-membrane calcium-activated potassium channels. These excitatory and inhibitory actions of ACh could be switched between by brief periods of NGFC action potential firing. Paired recordings demonstrated that cholinergic inhibition of NGFCs disinhibited the apical dendrites of layer 2/3 pyramidal neurons by silencing widespread, GABA B receptor-mediated, monosynaptic inhibition. Together, these data suggest that the cholinergic system modulates layer 1 inhibitory circuits in an activity-dependent manner to dynamically control dendritic synaptic inhibition of pyramidal neurons.

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Bioluminescence calcium imaging of network dynamics and their cholinergic modulation in slices of cerebral cortex from male rats

Tricoire

Drobac

Tsuzuki

et al. 2019

J of Neuroscience Research

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The activity of neuronal ensembles was monitored in neocortical slices from male rats using wide‐field bioluminescence imaging of a calcium sensor formed with the fusion of green fluorescent protein and aequorin (GA) and expressed through viral transfer. GA expression was restricted to pyramidal neurons and did not conspicuously alter neuronal morphology or neocortical cytoarchitecture. Removal of extracellular magnesium or addition of GABA receptor antagonists triggered epileptiform flashes of variable amplitude and spatial extent, indicating that the excitatory and inhibitory networks were functionally preserved in GA‐expressing slices. We found that agonists of muscarinic acetylcholine receptors largely increased the peak bioluminescence response to local electrical stimulation in layer I or white matter, and gave rise to a slowly decaying response persisting for tens of seconds. The peak increase involved layers II/III and V and did not result in marked alteration of response spatial properties. The persistent response involved essentially layer V and followed the time course of the muscarinic afterdischarge depolarizing plateau in layer V pyramidal cells. This plateau potential triggered spike firing in layer V, but not layer II/III pyramidal cells, and was accompanied by recurrent synaptic excitation in layer V. Our results indicate that wide‐field imaging of GA bioluminescence is well suited to monitor local and global network activity patterns, involving different mechanisms of intracellular calcium increase, and occurring on various timescales.

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Prolonged Disynaptic Inhibition in the Cortex Mediated by Slow, Non-α7 Nicotinic Excitation of a Specific Subset of Cortical Interneurons

Cited by 137 publications

References 33 publications

Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition

Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition

Activity-Dependent Modulation of Layer 1 Inhibitory Neocortical Circuits by Acetylcholine

Bioluminescence calcium imaging of network dynamics and their cholinergic modulation in slices of cerebral cortex from male rats

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