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Complete Dissertation VU Research Portal Cholinergic modulation of microcircuits in the cortex Obermayer, J.M.G. 2019 document version Publisher's PDF, also known as Version of record Link to publication in VU Research Portal citation for published version (APA) Obermayer, J. M. G. (2019). Cholinergic modulation of microcircuits in the cortex. General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. E-mail address: [email protected] Download date: 04. Oct. 2021 Cholinergic modulation of microcircuits in the cortex Joshua Obermayer The research described in this thesis was conducted at the department of Integrative Neurophysiology of the Center for Neurogenomics and Cognitive Research, Neuroscience Campus Amsterdam, Vrije Universiteit Amsterdam, the Netherlands. No part of this thesis may be reproduced without prior permission of the author. Front cover: shows two pyramidal neurons and an interneuron that together form a disynaptic inhibitory microcircuit in the human cortex. Tim Kroon reconstructed the neurons and Amber Kerkhofs made the cover design. VRIJE UNIVERSITEIT Cholinergic modulation of microcircuits In the cortex ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad Doctor aan de Vrije Universiteit Amsterdam, op gezag van de rector magnificus prof.dr. V. Subramaniam, in het openbaar te verdedigen ten overstaan van de promotiecommissie van de Faculteit der Bètawetenschappen op woensdag 3 april 2019 om 11.45 uur in de aula van de universiteit, De Boelelaan 1105 door Joshua Miro Gabriel Obermayer geboren te Rauenberg, Duitsland promotor: prof.dr. H.D. Mansvelder copromotor: dr. C.P.J. de Kock Table of contents Chapter 1 General introduction 7 Chapter 2 Prefrontal cortical ChAT-VIP interneurons 23 provide local excitation by cholinergic synaptic transmission and control attention Chapter 3 Layer-specific cholinergic control of human 47 and mouse cortical synaptic plasticity Chapter 4 Lateral inhibition by Martinotti interneurons 67 is facilitated by cholinergic inputs in human and mouse neocortex Chapter 5 General discussion 91 References 101 English summary 121 Nederlandse samenvatting 125 Acknowledgements 129 List of Publications 133 1 General introduction Elements of this text have been published in: Frontiers in Neural Circuits. 2017 December, 8;11:100 Obermayer J*, Verhoog MB*, Luchicchi A, Mansvelder HD. *Equal contribution Chapter 1 1.1 Attention The ability of the neocortex to construct a coherent representation of the outside world enables us to adapt to changes in our environment and to reach our goals. To do this, our brain has to combine sensory inputs from the outside world with our internal memories, action plans and expectations (Buschman and Miller, 2010). However, this is not an easy task: the amount of sensory inputs received in the sensory areas of our cortex is overwhelming and even the remarkable processing capabilities of the cortex cannot process all of them simultaneously. To compensate for this limitation, our brain developed a mechanism called attention to select and highlight relevant items at the expense of irrelevant ones (Sarter et al., 2001). To be able to determine at any given time point what item to focus on, our mind needs to combine external inputs with intrinsic goals (Sarter et al., 2001). For that, there are two mechanisms that control attention. The so-called “bottom up” or stimulus-driven attention describes a phenomenon where an external stimulus is noticed and leads us to instantly focus on it, for example an unexpected loud tone. The second mechanism is called “top-down” attention and means that we direct our focus based on our internal deliberations mainly independent from external inputs (Buschman and Miller, 2010; Corbetta and Shulman, 2002). These mechanisms are not excluding each other, but act in an overlapping manner (Egeth and Yantis, 1997). This makes it, for example, possible to stay focused and continue with reading an important e-mail, even when the person next to you has a loud conversation on the phone. Most research on the mechanisms behind attentional performance is done in human beings using EEG or imaging methods. A specific focus in these studies is on the prefrontal structures of the cortex since people who experience a damage of these structures show a reduced capability of impulse control and attention performance (Duncan et al., 1996; Miller, 2000). The most known example is probably the case of Phineas Gage, an American railroad construction foreman who survived an accident in which an iron rod damaged his frontal lobe. Eventually, this resulted in a change of his personality, affecting mainly his impulsivity and capability to stay focused (Macmillan, 2000). It is shown that patients with a damaged frontal cortex indeed have a decreased capability to attain future goals (Bechara et al., 1994) and that they get easily distracted by irrelevant features which catch their attention and prevent them from staying focused (Duncan et al., 1996; Miller, 2000). The capability to stay focused on a specific task for a long period of time is crucial for reaching long term goals and is described as sustained attention (Kim et al., 2016; Miller and Buschman, 2013; Sarter et al., 2001). Since this requires the suppression of external non-relevant stimuli and focus on the relevant input based on internal deliberations it is suggested that a “top-down” control of attention is crucial for sustained attentional performance (Buschman and Kastner, 2015; Miller and Buschman, 2013; Sarter et al., 2001). Recent studies using functional imaging methods in human beings or invasive recordings techniques in rodents and non-human primates, linked neuronal processing in the frontal cortex with sustained attention performance (Buschman and Kastner, 2015; Kim et al., 2016). For example, behavioral studies in rodents using a well- validated task for sustained attention performance: the 3- or 5 choice serial reaction time task (3/5CSRTT) (Lustig et al., 2013; Robbins, 2002) has shown that both activity of inhibitory interneurons as well as excitatory pyramidal neurons in the mPFC are crucial for proper sustained attention performance (Kim et al., 2016; Luchicchi et al., 2016). Taken together, sustained attentional performance is one of the key features to be capable to focus on the relevant information that our cortex receives. The processing of information occurs in neuronal networks in our brain. How attentional performance affect these networks will be further described in the following paragraph. 8 General introduction 1.2 The effect of attention demanding behavior on neuronal activity Neuronal networks are thought to represent behavioral states or sensory inputs through their specific firing activity. Indeed, it has been shown that a higher demand of attention 1 performance by adding distracters or decreasing the conspicuity of cues during a task led to an increased neuronal activity in the mPFC (Gill et al., 2000). This change of firing activity is thought to be caused by different populations of neurons that are in competition and either represent or do not represent the attended features, objects or locations (Reynolds et al., 1999; Thiele and Bellgrove, 2018). Recent studies indicate that population of neurons that represent attended objects, locations or features in general, increase their firing activity (Krauzlis et al., 2013; Noudoost et al., 2010; Thiele and Bellgrove, 2018). In contrast, neurons that represent irrelevant features had a reduced spiking activity (Martinez-Trujillo and Treue, 2004). How these neuronal networks exactly encode attention performance and affect behavior is not unraveled yet, but computational models give an insight by describing the effect of attention on neuronal input output relationships (Ni and Maunsell, 2017; Ni et al., 2012; Sanayei et al., 2015). The effect of attention on these relationships are described by a “gain change” (Ni et al., 2012; Sanayei et al., 2015). In the “normalization model of attention” it is assumed that attention affects the gain of both excitatory and inhibitory neurons (Ni and Maunsell, 2017; Ni et al., 2012; Sanayei et al., 2015). In that way the increased activity of excitatory neurons is normalized by the higher excitation of inhibitory neurons (Ni and Maunsell, 2017; Ni et al., 2012). Recent in vivo studies in macaque monkeys and rodents indicated indeed that both the activity of excitatory as well as inhibitory neurons in the frontal cortex is increased while the animal performs an attention demanding behavior (Kim et al., 2016; Thiele et al., 2016). These findings indicate the importance of both excitatory as well as inhibitory neuron activity during attention demanding behavior to maintain the excitation inhibition balance. On a network level, attention demanding behavior correlates with
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