Paying attention to the thalamic reticular nucleus

doi:10.1016/S0166-2236(97)01157-0

Trends in Neurosciences

Volume 21, Issue 1, 1 January 1998, Pages 28-32

https://doi.org/10.1016/S0166-2236(97)01157-0 Get rights and content

Abstract

The thalamic reticular nucleus can be divided into a number of sectors, each concerned with a different function (sight, touch, hearing, movement or `limbic' functions). Each sector is connected to more than one thalamic nucleus and to more than one cortical area, and each sector has topographically mapped connections with the thalamus and the cortex. We consider the known details of these connections and show: (1) that they are not the same for each sector; (2) that the reticular nucleus serves as a nexus, where several functionally related cortical areas and thalamic nuclei can interact, modifying thalamocortical transmission through the inhibitory connections that go from the reticular cells to thalamic relay cells; and (3) that we need much more detailed information about these highly organized connections before we can understand exactly how the thalamic reticular nucleus might be influencing thalamocortical pathways in attentional mechanisms or in other, as yet undefined, roles.

Section snippets

Multiple inputs to single sectors of TRN

For any single functional thalamocortical pathway and its related TRN sector, there is usually more than one connected thalamic nucleus or cortical area. Thus, visual, auditory and somatosensory systems have many cortical areas22, 23, 24 and more than one related thalamic nucleus connected to TRN (6, 9, 10, 11, 12). The way in which several thalamocortical circuits relate to each other in TRN must be crucial to the influence that any one cortical area can exert on the modulation going from a

Functional implications

At present, evidence on details of reticular connections is incomplete. One reason for writing this article is to stress the importance of defining the connections. It is clear that no simple general rule governing cortical and thalamic connections in TRN applies to all sectors. Each sector appears to follow distinct rules. To understand how any one sector responds to its several inputs and then produces modulatory effects in the thalamus, we have to look at its particular pattern of

Concluding remarks

The organization of TRN involves the interaction of several thalamocortical circuits for each functionally distinct sector of TRN. We have discussed two cortical areas and two thalamic nuclei for each sector, but generally more cortical areas and more thalamic nuclei are involved in any one sector. The important point is that each sector provides a nexus for the interaction of several thalamocortical and corticothalamic circuits, and will prove to be a key site where many cortical areas

Acknowledgements

This work was supported by grants from the Wellcome Trust and the NIH (EY11494). We thank Dr D. Pinault for a critical reading of the manuscript.

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The thalamic reticular nucleus (TRN) is a thin sheet of GABAergic neurons surrounding the thalamus, and it regulates the activity of thalamic relay neurons. The TRN has been reported to be involved in sensory gating, attentional regulation, and some other functions. However, little is known about the contribution of the TRN to sequence learning. In the present study, we examined whether the TRN is involved in reward-based learning of action sequence with no eliciting stimuli (operant conditioning), by analyzing the performance of male and female Avp-Vgat^−/− mice (Vgat^flox/flox mice crossed to an Avp-Cre driver line) on tasks conducted in an operant box having three levers. Our histological and electrophysiological data demonstrated that in adult Avp-Vgat^−/− mice, vesicular GABA transporter (VGAT) was absent in most TRN neurons and the GABAergic transmission from the TRN to the thalamus was largely suppressed. The performance on a task in which mice needed to press an active lever for food reward showed that simple operant learning of lever pressing and learning of win-stay and lose-shift strategies are not affected in Avp-Vgat^−/− mice. In contrast, the performance on a task in which mice needed to press three levers in a correct order for food reward showed that learning of the order of lever pressing (action sequence learning) was impaired in Avp-Vgat^−/− mice. These results suggest that the TRN plays an important role in action sequence learning.
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Planar cell polarity (PCP) signaling plays a fundamental role in shaping the development and ongoing function of the nervous system, beginning from early stages of neural tube closure and spanning the maintenance of functional synapses in adults. While mutations in core PCP signaling proteins have long been suspected to underlie neural tube closure defects in humans, recent findings also implicate their potential involvement in neurodevelopmental and neuropsychiatric disorders. Missense and loss-of-function mutations in CELSR3, a core component of PCP signaling complexes, are highly associated with Tourette Disorder. Although the functional significance of these mutations has yet to be elucidated in animal and cell models, the expression patterns of Celsr3 in mice point to alterations in cortico-striato-thalamo-cortical circuits. Here, we briefly review the known functions of Celsr3 for nervous system development. We also propose circuit models for Tourette Disorder by hypothesizing roles for Celsr3 in controlling striatal neuromodulation via effects on cholinergic interneurons, and thalamic inhibition through its functions in thalamic reticular nuclei. Testing these and related hypotheses in animal and cell models will move us closer to unraveling the neuropathogenesis of Tourette Disorder, with the ultimate goal of developing more efficacious treatments for both motor and cognitive symptoms.
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There is no doubt on the participation of the thalamus in the various types of genetic generalized epilepsies as evidenced by multiple non-invasive imaging studies in humans as well as invasive studies in animal models of GGE. Based on human and mostly animal data gathered in early 2000 a so called ‘three compartment model’ on seizure generation was proposed conceptualizing the existence of a hyperexcitable cortical seizure onset zone providing excitation to relay cells of the relay thalamus and the inhibitory reticular thalamic nucleus (RTn). The interplay of corticothalamic excitation and feedforward inhibition via RTn is supposed to entrain thalamic relay neurons into synchronous, oscillatory activity for SWD sustainment. With the emergence of more fine-tuned experimental techniques and analyses, however, it becomes apparent that this model is too simplistic as the thalamus cannot be regarded as unity. Rather, different thalamic nuclei, being integrated in different thalamocortical and other subcortical subloops, need to be differentiated, which take over different functions for seizure generation, generalization and maintenance. Moreover, these networks are not necessarily the same for different classes of patients with GGE and can even be antagonistic between seizure types. This review will summarize data concerning different nuclei and their participation in GGE in order to extend this model and create a more detailed concept on seizure generation, generalization and maintenance.
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Citation Excerpt :
Primarily for hippocampal spindles, although the literature that has studied them is considerable (Brazier, 1968, 1970, 1972; Crowne and Radcliffe, 1975; Moiseeva and Aleksanyan, 1976; Lopes da Silva and Arnolds, 1978; Halgren et aI., 1978; Ravagnati et al., 1979; Montplaisir et al., 1980; Sarasso et al., 2014; Frauscher et al., 2015b; Frauscher and Dubeau, 2018; von Ellenrieder et al., 2020), including studies regarding their potential functional significance (Marshall and Born, 2007; Clemens et al., 2011; Ferrara et al., 2012), there has been no actual evidence that they are normal iEEG entities. It is their morphological resemblance to scalp EEG sleep spindles that has biased literature and iEEG reviewers until now in considering hippocampal spindles as normal neurophysiological oscillations, although it is well documented that the scalp sleep spindles result from thalamo-cortical interactions (Guillery et al., 1998; Jones, 1998; Steriade 1999, 2000, 2003; Astori et al., 2011; Halassa et al., 2011) while the hippocampal spindles are intrinsic to the hippocampus (Crowne and Radcliffe, 1975; Moiseeva and Aleksanyan, 1976; Lopes da Silva and Arnolds, 1978; Halgren et aI., 1978; Ravagnati et al., 1979; Montplaisir et al., 1980). Secondarily for the recently recognized hippocampal barques, although our previous study demonstrated their temporal correlation to ctenoids in non-epileptogenic hippocampi from patients with xTLE (Kokkinos et al, 2019), the argument that the intracranial correlate can share the properties of its scalp manifestation is rather weak; alternative explanations suggest that epileptiform iEEG entities may constitute markers of higher risk to develop hippocampal epileptogenicity later in life (Issa et al., 2018; Chen et al., 2020).
To assess whether hippocampal spindles and barques are markers of epileptogenicity.
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Both spindles and barques are normal entities of the hippocampal intracranial electroencephalogram. The presence of barques may also signify lack of epileptogenic properties in the hippocampus.
Understanding that hippocampal spindles and barques do not reflect epileptogenicity is critical for correct interpretation of epilepsy surgery evaluations and appropriate surgical treatment selection.
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Trends in Neurosciences

Paying attention to the thalamic reticular nucleus

Abstract

Section snippets

Multiple inputs to single sectors of TRN

Functional implications

Concluding remarks

Acknowledgements

Brain Res

Brain Res

Prog. Neurobiol

Neuroscience

Trends Neurosci

Neuroscience

Neuroscience

Hearing Res

Trends Neurosci

Brain Res

Brain Res. Bull

Curr. Opinion Neurobiol

Proc. Natl. Acad. Sci. U. S. A

The Thalamus,

J. Neurocytol

Science

Eur. J. Neurosci

Eur. J. Neurosci

Eur. J. Neurosci

J. Comp. Neurol

Eur. J. Neurosci

Eur. J. Neurosci