Somatostatin-Expressing Interneurons Enable and Maintain Learning-Dependent Sequential Activation of Pyramidal Neurons

Adler, Avital; Zhao, Ruohe; Shin, Myung Eun; Yasuda, Ryohei; Gan, Wen‐Biao

doi:10.1016/j.neuron.2019.01.036

Cited by 135 publications

(144 citation statements)

References 65 publications

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“…Many studies have shown that the different subtypes of interneurons display different activation patterns in learned behaviours and characteristic behavioural states, and they are important players in neuroplasticity (Gentet et al 2012;Hensch 2005;Katona et al 2014;Lee et al 2012;Nys et al 2015;Pinto and Dan 2015;Sachidhanandam et al 2016;Schneider et al 2014). SST INs have been found to be involved in the cellular mechanisms of learning (Adler et al 2019;Chen et al 2015;Cichon and Gan 2015;Kato et al 2015;Letzkus et al 2011;Lovett-Barron et al 2014;McKay et al 2013;Pi et al 2013;Stefanelli et al 2016;Wolff et al 2014) and cortical plasticity (Fu et al 2015;Khan et al 2018;Scheyltjens and Arckens 2016). Our studies of learning-dependent plasticity in the barrel cortex point to the involvement of SST containing GABAergic neurons in the mechanism underlying the development of plastic changes (Cybulska-Klosowicz et al 2013).…”

Section: Introductionmentioning

confidence: 72%

Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

et al. 2019

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Inhibitory interneurons in the cerebral cortex contain specific proteins or peptides characteristic for a certain interneuron subtype. In mice, three biochemical markers constitute non-overlapping interneuron populations, which account for 80-90% of all inhibitory cells. These interneurons express parvalbumin (PV), somatostatin (SST), or vasoactive intestinal peptide (VIP). SST is not only a marker of a specific interneuron subtype, but also an important neuropeptide that participates in numerous biochemical and signalling pathways in the brain via somatostatin receptors (SSTR1-5). In the nervous system, SST acts as a neuromodulator and neurotransmitter affecting, among others, memory, learning, and mood. In the sensory cortex, the co-localisation of GABA and SST is found in approximately 30% of interneurons. Considering the importance of interactions between inhibitory interneurons in cortical plasticity and the possible GABA and SST co-release, it seems important to investigate the localisation of different SSTRs on cortical interneurons. Here, we examined the distribution of SSTR1-5 on barrel cortex interneurons containing PV, SST, or VIP. Immunofluorescent staining using specific antibodies was performed on brain sections from transgenic mice that expressed red fluorescence in one specific interneuron subtype (PV-Ai14, SST-Ai14, and VIP-Ai14 mice). SSTRs expression on PV, SST, and VIP interneurons varied among the cortical layers and we found two patterns of SSTRs distribution in L4 of barrel cortex. We also demonstrated that, in contrast to other interneurons, PV cells did not express SSTR2, but expressed other SSTRs. SST interneurons, which were not found to make chemical synapses among themselves, expressed all five SSTR subtypes.

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Section: Introductionmentioning

confidence: 72%

Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

et al. 2019

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“…We found that most AId neurons were selective for single movements or for different AId of anesthetized zebra finches elicits increased spontaneous firing rates, and parvalbumin expression is higher in AId compared to surrounding motor cortex (Mello et al, 2019;Yuan and Bottjer, 2019). Similarly, mammalian motor cortex contains a substantial population of inhibitory interneurons, which have been implicated in both regulating plasticity during motor skill learning and coordinating activity across motor cortex during behavior (Jacobs and Donoghue, 1991;Hess and Donoghue, 1994;Hess et al, 1996;Markram et al, 2004;Stagg et al, 2011;Donato et al, 2013;Chen et al, 2015;Kida et al, 2016;Adler et al, 2019). Studies have suggested that blocking inhibition unmasks latent excitatory connections between spatially distant motor cortical neurons, providing a mechanism by which dynamic modulation of inhibition could flexibly reorganize connectivity and coordinate population activity across motor cortex (Jacobs and Donoghue, 1991;Spiro et al, 1999;Schneider et al, 2002;Capaday, 2004).…”

Section: Heterogeneous Activity Within Aid Suggests Multi-dimensionalmentioning

confidence: 93%

Multi-dimensional tuning in motor cortical neurons during active behavior

Yuan

Bottjer

2020

Preprint

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A region within songbird cortex, AId (dorsal intermediate arcopallium), is functionally analogous to motor cortex in mammals and has been implicated in vocal learning during development. AId thus serves as a powerful model for investigating motor cortical contributions to developmental skill learning. We made extracellular recordings in AId of freely behaving juvenile zebra finches and evaluated neural activity during diverse motor behaviors throughout entire recording sessions, including song production as well as hopping, pecking, preening, fluffups, beak interactions with cage objects, scratching, and stretching. A large population of single neurons showed significant modulation of activity during singing relative to quiescence. In addition, AId neurons demonstrated heterogeneous response patterns that were evoked during multiple movements, with single neurons often demonstrating excitation during one movement type and suppression during another. Lesions of AId do not disrupt vocal motor output or impair generic movements, suggesting that the responses observed during active behavior do not reflect direct motor drive. Consistent with this idea, we found that some AId neurons showed differential activity during pecking movements depending on the context in which pecks occurred, suggesting that AId circuitry encodes diverse inputs beyond generic motor parameters.Moreover, we found evidence of neurons that did not respond during discrete movements but were nonetheless modulated during active behavioral states compared to quiescence. Taken together, our results support the idea that AId neurons are involved in sensorimotor integration of external sensory inputs and/or internal feedback cues to help modulate goal-directed behaviors. SIGNIFICANCE STATEMENTMotor cortex across taxa receives highly integrated, multi-modal information and has been implicated in both execution and acquisition of complex motor skills, yet studies of motor cortex typically employ restricted behavioral paradigms that target select movement parameters, preventing wider assessment of the diverse sensorimotor factors that can affect motor cortical activity. Recording in AId of freely behaving juvenile songbirds that are actively engaged in sensorimotor learning offers unique advantages for elucidating the functional role of motor cortical neurons. The results demonstrate that a diverse array of factors modulate motor cortical activity and lay important groundwork for future investigations of how multi-modal information is integrated in motor cortical regions to contribute to learning and execution of complex motor skills.3

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“…SST is expressed in subsets of GABAergic interneurons of the mammalian pallium (hippocampus, cortex) and appears to play a key role in their inhibitory circuits (Urban-Ciecko and Barth, 2016;Adler, Zhao, Shin, Yasuda, & Gan, 2019). Moreover, a number of subpopulations of SST neurons can be distinguished by morphology, connectivity, laminar location, firing properties, and expression of molecular markers (Yavorska and Wehr, 2016).…”

Section: Wide But Differential Expression Of Psst1 and Psst6 Genes Inmentioning

confidence: 99%

Differential expression of five prosomatostatin genes in the central nervous system of the catsharkScyliorhinus canicula

Sobrido‐Cameán

Tostivint²,

Mazan

et al. 2019

Preprint

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Five prosomatostatin genes (PSST1, PSST2, PSST3, PSST5 and PSST6) have been recently identified in elasmobranchs (Tostivint, Gaillard, Mazan, & Pézeron, 2019). In order to gain insight into the contribution of each somatostatin to specific nervous systems circuits and behaviors in this important jawed vertebrate group, we studied the distribution of neurons expressing PSST mRNAs in the catshark Scyliorhinus canicula using in situ hybridization with specific probes for the five PSSTs transcripts. Additionally, we combined in situ hybridization with tyrosine hydroxylase (TH) immunochemistry for better localization of some PSSTs-positive populations. The five PSST genes showed expression in the brain, although with important differences in distribution. PSST1 and PSST6 were widely expressed in different brain regions. Instead, PSST2 and PSST3 were expressed only in the ventral hypothalamus and in some hindbrain lateral reticular neurons, whereas PSST5 was only expressed in the region of the entopeduncular nucleus. PSST1 and PSST6 were expressed by numerous pallial neurons, although in different populations judging from the colocalization of tyrosine hydroxylase (TH) immunoreactivity and PSST6 expression in pallial neurons and the absence of colocalization between TH and PSST1 expression. Differential expression of PSST1 and PSST6 was also observed in the subpallium, hypothalamus, diencephalon, optic tectum, midbrain tegmentum and rhombencephalon. Expression of PSST1 was observed in numerous cerebrospinal fluid-contacting (CSF-c) neurons of the paraventricular organ of the hypothalamus and the central canal of the spinal cord.These wide differences in expression of PSST genes together with the numerous brain nuclei expressing PSSTs, indicate that catshark somatostatinergic neurons are implicated differentially in a number of neural circuits.

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Somatostatin-Expressing Interneurons Enable and Maintain Learning-Dependent Sequential Activation of Pyramidal Neurons

Cited by 135 publications

References 65 publications

Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

Multi-dimensional tuning in motor cortical neurons during active behavior

Differential expression of five prosomatostatin genes in the central nervous system of the catsharkScyliorhinus canicula

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