Thalamic Neuromodulation and Its Implications for Executive Networks

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Thalamic Neuromodulation and Its Implications for Executive Networks Thalamic neuromodulation and its implications for executive networks The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation Varela, Carmen. “Thalamic Neuromodulation and Its Implications for Executive Networks.” Front. Neural Circuits 8 (June 24, 2014). As Published http://dx.doi.org/10.3389/fncir.2014.00069 Publisher Frontiers Research Foundation Version Final published version Citable link http://hdl.handle.net/1721.1/89204 Terms of Use Creative Commons Attribution Detailed Terms http://creativecommons.org/licenses/by/4.0/ REVIEW ARTICLE published: 24 June 2014 doi: 10.3389/fncir.2014.00069 Thalamic neuromodulation and its implications for executive networks Carmen Varela* Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, MA, USA Edited by: The thalamus is a key structure that controls the routing of information in the brain. Guillermo Gonzalez-Burgos, Understanding modulation at the thalamic level is critical to understanding the flow of University of Pittsburgh, USA information to brain regions involved in cognitive functions, such as the neocortex, the Reviewed by: hippocampus, and the basal ganglia. Modulators contribute the majority of synapses Robert P.Vertes, Florida Atlantic University, USA that thalamic cells receive, and the highest fraction of modulator synapses is found in Randy M. Bruno, Columbia University, thalamic nuclei interconnected with higher order cortical regions. In addition, disruption USA of modulators often translates into disabling disorders of executive behavior. However, *Correspondence: modulation in thalamic nuclei such as the midline and intralaminar groups, which are Carmen Varela, Picower Institute for interconnected with forebrain executive regions, has received little attention compared Learning and Memory, Massachusetts Institute of Technology, Building 46, to sensory nuclei. Thalamic modulators are heterogeneous in regards to their origin, the Room 5233, 43 Vassar Street, neurotransmitter they use, and the effect on thalamic cells. Modulators also share some Cambridge, MA 02139, USA features, such as having small terminal boutons and activating metabotropic receptors e-mail: carmenv@mit.edu on the cells they contact. I will review anatomical and physiological data on thalamic modulators with these goals: first, determine to what extent the evidence supports similar modulator functions across thalamic nuclei; and second, discuss the current evidence on modulation in the midline and intralaminar nuclei in relation to their role in executive function. Keywords: modulators, acetylcholine, serotonin, dopamine, noradrenaline, histamine, midline, intralaminar INTRODUCTION AND KEY TERMS but each of them could also contribute to subthreshold modula- THALAMIC AFFERENTS: DRIVERS AND MODULATORS tion that is integrated across all drivers to generate an output, All the forebrain structures that contribute to cognitive functions something that will need to be tested. Similarly, some modulators receive input from the thalamus, which is a critical point for the outside of the primary sensory thalamus share features of drivers routing of information and gateway control. Thalamic cells receive (such as the large cholinergic afferents in some higher order nuclei, two general types of afferents, drivers and modulators. Thalamic reviewed below). Therefore, the definition of drivers and modu- drivers are afferents that target proximal dendrites with relatively lators that is used here is an operational definition that may need large synaptic boutons, reliably evoke spikes in thalamic cells, and refinement as we learn more about the thalamus. whose function is thought to be the faithful transmission of the In every thalamic nucleus studied to date, modulator synapses spike message relayed by thalamic cells to postsynaptic structures. are found to constitute the vast majority of inputs to a given relay In contrast, modulators are those afferents that target primarily cell. The innervation by modulators is particularly dense in the distal dendrites and influence spike transmission by adjusting the midline and intralaminar groups of thalamic nuclei, both inter- cellular and synaptic mechanisms underlying spike generation; by connected with executive areas such as the medial prefrontal cortex doing so, they are thought to fine-tune the message relayed by tha- (mPFC) and basal ganglia. mPFC and the basal ganglia have been lamic cells and control its probability of transmission (reviewed extensively studied, including the effect of modulators on these in Sherman and Guillery, 1998; Guillery and Sherman, 2002). It regions. Surprisingly, the midline and intralaminar nuclei are should be noted that this distinction between drivers and modula- largely unexplored territory compared to neocortex, basal gan- tors is largely based on evidence from the sensory thalamus, which glia, or the sensory thalamic nuclei. Even some basic questions, has critical relay functions. Outside of the sensory thalamus, the such as the cell response properties or the modulator effects on evidence (still scarce and mostly anatomical) suggests that the these thalamic nuclei, remain unanswered. This review will first anatomical features that distinguish drivers and modulators are discuss anatomical and physiological results on modulators across present in all thalamic nuclei, although the functional correlates the thalamus. In the second part, it will review recent evidence that regarding spike generation and transmission still need to be char- highlights the importance of midline and intralaminar nuclei in acterized for many thalamic regions. For example, nuclei outside executive functions, and the role of modulators in these nuclei. The the primary sensory thalamus receive afferents with driver mor- objective is to point out important gaps in knowledge and untested phology from multiple sources (Baldauf et al., 2005; Masterson hypotheses regarding the function of modulators in the thalamus. et al., 2009). These drivers converging onto individual cells may Recent technological developments (optogenetics, pharmacoge- contribute to spike generation like the drivers in sensory thalamus, netics, clearing techniques such as “clarity”) provide powerful Frontiers in Neural Circuits www.frontiersin.org June 2014 | Volume 8 | Article 69 | 1 Varela Thalamic modulators and executive function tools to address many open questions that must be answered in neurotransmitters, for example, on gene expression, synaptogene- order to elucidate the role of thalamic modulation in executive sis, local blood flow, etc. Because of their broad spectrum of actions networks. they fall far from the scope of this review. Similarly, other uncon- Modulators constitute a heterogeneous group of afferents that ventional neurotransmitters like endocannabinoids, purines, and nevertheless share some anatomical and physiological properties nitric oxide are present in the terminals of some thalamic afferents across the thalamus (reviewed in Sherman and Guillery, 1998; (reviewed in Jones, 2007), but their effects will not be examined Figure 1A). Modulators originate in a variety of brain regions here. and use various neurotransmitters (summarized schematically in Figure 1B). Examples of thalamic modulators include cholinergic, THALAMIC NUCLEI: FIRST AND HIGHER ORDER serotonergic, dopaminergic, and noradrenergic afferents from the Guillery (1995) distinguished two groups of thalamic nuclei: brainstem, histaminergic afferents from the hypothalamus, and “First order” are those nuclei that receive drivers from ascend- glutamatergic afferents from layer VI of neocortex. ing afferent pathways, and transmit information that arrives The first part of this review will discuss the anatomy and at the thalamus for the first time. Nuclei in the other group physiology of six chemically defined modulators across the tha- were named “higher order,” and are those that relay informa- lamus. GABAergic inputs to thalamic nuclei, which originate tion that has gone through the thalamus at least once (through primarily from diencephalic sources, will not be considered in a first order nucleus). The main feature that distinguishes higher this review. Furthermore, many neuroactive peptides (including from first order nuclei is that at least some of their driver input orexins) co-localize with neurotransmitter systems in the thala- originates in layer V of neocortex; for this reason, they are mus (reviewed in Jones, 2007), and can have wider effects than thought to participate in cortico-cortical communication (Theyel FIGURE 1 | General properties of thalamic afferents. (A) Schematic which it has been tested, the postsynaptic responses facilitate under representation of the features that distinguish drivers and modulators in first repetitive stimulation. (B) Approximate location of the brain regions that order (left) and higher order (right) nuclei. Note the higher fraction of provide modulator afferents to the thalamus, color-coded for the modulators in higher order nuclei, where some modulators have large neurotransmitter they use. The outline of a rodent brain is used for synapses contacting proximal dendrites. In both first and higher order nuclei, convenience, although the diagram combines results from different species modulators activate ionotropic and metabotropic receptors and, in those in (see text for details). Frontiers in Neural Circuits www.frontiersin.org June 2014 | Volume 8 | Article 69
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