Visual-Induced Excitation Leads to Firing Pauses in Striatal Cholinergic Interneurons

Schulz, Jan M.; Oswald, Manfred J.; Reynolds, John N. J.

doi:10.1523/jneurosci.0661-11.2011

Cited by 40 publications

(50 citation statements)

References 50 publications

(96 reference statements)

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“…In monkey behavior studies, the CINs display a pause in their tonic firing activity after a conditioned stimulus, which becomes salient when it links to reward (Aosaki et al, 1994; Morris et al, 2004; Joshua et al, 2008). A similar pause in firing of the CINs has also been observed in rats (Schulz et al, 2011) and mice (Ding et al, 2010; Straub et al, 2014). The mechanisms underlying the pause in firing of the CINs might be suppression from midbrain DA neurons (Morris et al, 2004; Chuhma et al, 2014; Straub et al, 2014), inhibition from VTA GABA neurons (Brown et al, 2012), or glutamatergic excitation from thalamus-generated intrinsic afterhyperpolarization (Schulz et al, 2011).…”

Section: Expected Results: Optogenetic Studies Demonstrating Direct Tsupporting

confidence: 77%

“…A similar pause in firing of the CINs has also been observed in rats (Schulz et al, 2011) and mice (Ding et al, 2010; Straub et al, 2014). The mechanisms underlying the pause in firing of the CINs might be suppression from midbrain DA neurons (Morris et al, 2004; Chuhma et al, 2014; Straub et al, 2014), inhibition from VTA GABA neurons (Brown et al, 2012), or glutamatergic excitation from thalamus-generated intrinsic afterhyperpolarization (Schulz et al, 2011). ACh and DA are well known for their complementary role in maintaining balance on signal integration in the striatum.…”

Section: Expected Results: Optogenetic Studies Demonstrating Direct Tsupporting

confidence: 77%

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Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system

Jiang¹,

López-Hernández²,

Lederman³

et al. 2014

Reviews in the Neurosciences

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AbstractMolecular manipulations and targeted pharmacological studies provide a compelling picture of which nicotinic receptor subtypes are where in the central nervous system (CNS) and what happens if one activates or deletes them. However, understanding the physiological contribution of nicotinic receptors to endogenous acetylcholine (ACh) signaling in the CNS has proven a more difficult problem to solve. In this review, we provide a synopsis of the literature on the use of optogenetic approaches to control the excitability of cholinergic neurons and to examine the role of CNS nicotinic ACh receptors (nAChRs). As is often the case, this relatively new technology has answered some questions and raised others. Overall, we believe that optogenetic manipulation of cholinergic excitability in combination with some rigorous pharmacology will ultimately advance our understanding of the many functions of nAChRs in the brain.

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Section: Expected Results: Optogenetic Studies Demonstrating Direct Tsupporting

confidence: 77%

Section: Expected Results: Optogenetic Studies Demonstrating Direct Tsupporting

confidence: 77%

Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system

Jiang¹,

López-Hernández²,

Lederman³

et al. 2014

Reviews in the Neurosciences

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“…Although the amplitude of state transitions varied between neurones, the pattern was very similar to those in SPNs in most cases, and distinctly different from membrane potential fluctuations in CINs (Fig. 2; a detailed analysis of the correlation with the ECoG can be found in Schulz et al . 2011).…”

Section: Resultsmentioning

confidence: 68%

Enhanced high‐frequency membrane potential fluctuations control spike output in striatal fast‐spiking interneurones in vivo

Schulz¹,

Pitcher²,

Savanthrapadian³

et al. 2011

The Journal of Physiology

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Non-technical Summary Rhythmic activity patterns are a common theme throughout neuroscience. However, it is still poorly understood how network functions are modulated by fast oscillatory inputs from distant brain regions. In this respect, the striatum is particularly interesting as almost all neuronal activity is driven by long-range inputs. We find that the three main classes of neurones in the striatum show very distinct oscillatory activity patterns in specific frequency ranges. In particular, we show that fast-spiking interneurones are highly sensitive to fast fluctuating synaptic inputs in the intact brain. This sensitivity was probably due to a combination of faster dynamics of synaptic inputs and intrinsic amplification of high-frequency signals. In contrast, projection neurones and other interneurones lacking these mechanisms were insensitive to fast oscillatory input patterns. These results suggest that transmission of fast cortical oscillatory inputs modulates information processing in the striatum via engagement of fast-spiking interneurones.Abstract Fast-spiking interneurones (FSIs) constitute a prominent part of the inhibitory microcircuitry of the striatum; however, little is known about their recruitment by synaptic inputs in vivo. Here, we report that, in contrast to cholinergic interneurones (CINs), FSIs (n = 9) recorded in urethane-anaesthetized rats exhibit Down-to-Up state transitions very similar to spiny projection neurones (SPNs). Compared to SPNs, the FSI Up state membrane potential was noisier and power spectra exhibited significantly larger power at frequencies in the gamma range (55-95 Hz). The membrane potential exhibited short and steep trajectories preceding spontaneous spike discharge, suggesting that fast input components controlled spike output in FSIs. Spontaneous spike data contained a high proportion (43.6 ± 32.8%) of small inter-spike intervals (ISIs) of <30 ms, setting FSIs clearly apart from SPNs and CINs. Cortical-evoked inputs had slower dynamics in SPNs than FSIs, and repetitive stimulation entrained SPN spike output only if the stimulation was delivered at an intermediate frequency (20 Hz), but not at a high frequency (100 Hz). Pharmacological induction of an activated ECoG state, known to promote rapid FSI spiking, mildly increased the power (by 43 ± 55%, n = 13) at gamma frequencies in the membrane potential of SPNs, but resulted in few small ISIs (<30 ms; 4.3 ± 6.4%, n = 8). The gamma frequency content did not change in CINs (n = 8). These results indicate that FSIs are uniquely responsive to high-frequency input sequences. By controlling the spike output of SPNs, FSIs could serve gating of top-down signals and long-range synchronisation of gamma-oscillations during behaviour.(Received 27 May 2011; accepted after revision 6 July 2011; first published online 11 July 2011) Corresponding author J. M. Schulz: Department of Physiology, University of Bern, Bühlplatz 5, 3012 Bern, Switzerland. Email: schulz@pyl.unibe.ch Abbreviations AP, anterior-posterior from bregma; BIC...

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“…The TANs receive excitatory inputs from cortex and thalamus, and have been shown to increase their discharge in response to direct cortical stimulation (Sharott et al, 2012). Although TANs receive both cortical and thalamic innervations, the TAN characteristic pause response is probably driven by thalamic input (Matsumoto et al, 2001; Nanda et al, 2009; Ding et al, 2010; Schulz et al, 2011). …”

Section: Introductionmentioning

confidence: 99%

Different correlation patterns of cholinergic and GABAergic interneurons with striatal projection neurons

Adler¹,

Katabi²,

Finkes³

et al. 2013

Front. Syst. Neurosci.

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The striatum is populated by a single projection neuron group, the medium spiny neurons (MSNs), and several groups of interneurons. Two of the electrophysiologically well-characterized striatal interneuron groups are the tonically active neurons (TANs), which are presumably cholinergic interneurons, and the fast spiking interneurons (FSIs), presumably parvalbumin (PV) expressing GABAergic interneurons. To better understand striatal processing it is thus crucial to define the functional relationship between MSNs and these interneurons in the awake and behaving animal. We used multiple electrodes and standard physiological methods to simultaneously record MSN spiking activity and the activity of TANs or FSIs from monkeys engaged in a classical conditioning paradigm. All three cell populations were highly responsive to the behavioral task. However, they displayed different average response profiles and a different degree of response synchronization (signal correlation). TANs displayed the most transient and synchronized response, MSNs the most diverse and sustained response and FSIs were in between on both parameters. We did not find evidence for direct monosynaptic connectivity between the MSNs and either the TANs or the FSIs. However, while the cross correlation histograms of TAN to MSN pairs were flat, those of FSI to MSN displayed positive asymmetrical broad peaks. The FSI-MSN correlogram profile implies that the spikes of MSNs follow those of FSIs and both are driven by a common, most likely cortical, input. Thus, the two populations of striatal interneurons are probably driven by different afferents and play complementary functional roles in the physiology of the striatal microcircuit.

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Visual-Induced Excitation Leads to Firing Pauses in Striatal Cholinergic Interneurons

Cited by 40 publications

References 50 publications

Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system

Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system

Enhanced high‐frequency membrane potential fluctuations control spike output in striatal fast‐spiking interneurones in vivo

Different correlation patterns of cholinergic and GABAergic interneurons with striatal projection neurons

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