The thalamic reticular nucleus: structure, function and concept

doi:10.1016/j.brainresrev.2004.04.008

Brain Research Reviews

Volume 46, Issue 1, August 2004, Pages 1-31

https://doi.org/10.1016/j.brainresrev.2004.04.008 Get rights and content

Abstract

On the basis of theoretical, anatomical, psychological and physiological considerations, Francis Crick (1984) proposed that, during selective attention, the thalamic reticular nucleus (TRN) controls the internal attentional searchlight that simultaneously highlights all the neural circuits called on by the object of attention. In other words, he submitted that during either perception, or the preparation and execution of any cognitive and/or motor task, the TRN sets all the corresponding thalamocortical (TC) circuits in motion. Over the last two decades, behavioural, electrophysiological, anatomical and neurochemical findings have been accumulating, supporting the complex nature of the TRN and raising questions about the validity of this speculative hypothesis. Indeed, our knowledge of the actual functioning of the TRN is still sprinkled with unresolved questions. Therefore, the time has come to join forces and discuss some recent cellular and network findings concerning this diencephalic GABAergic structure, which plays important roles during various states of consciousness. On the whole, the present critical survey emphasizes the TRN's complexity, and provides arguments combining anatomy, physiology and cognitive psychology.

Section snippets

Virtually all functional modalities

The TRN is concerned with almost if not all functional modalities. Moreover, electrophysiological studies have demonstrated the existence of at least seven sectors in the TRN, five sensory (auditory, gustatory, somatosensory, visceral and visual), one motor and one limbic. Shosaku et al. [234], [235] performed comprehensive physiological studies in the rat showing the topographic organization of the somatosensory, auditory (also see Ref. [267]) and visual sectors (Fig. 2). The large size of the

Receptive field properties

Reticular cells generally have larger receptive fields than TC neurons [207], [224], [240], [260], [277], [279]. Although the experimental conditions (e.g., type and depth of anaesthesia) modulate the characteristics of the receptive field(s) of any given neuron in some way, the data currently to hand demonstrate that a small percentage of TRN cells can respond to two sensory modalities, probably those that are located within a region that is common to two adjacent sectors. Moreover, the

Diverse somatodendritic architectures

From a morphological viewpoint, it is not yet clear whether the TRN contains a homogeneous or heterogeneous cellular population. When investigating the architecture of rabbit and mouse TRN cells with the silver chromate method, Ramon y Cajal [212] highlighted the long hairy and sparsely divided dendritic processes emerging from a fusiform or triangular cell body. Using Golgi impregnation of thalamic pieces of adult cats, Scheibel and Scheibel [226] identified tightly packed dendritic bundles in

Cellular neurochemical diversities

The heterogeneity of the TRN has also been demonstrated using immunocytochemical stainings, in particular of Ca²⁺-binding proteins (calbindin, parvalbumin and calretinin), which are present in different subsets of TRN neurons in various species [37], [72], [77], [140], [161], [215], [274]. Calcium-binding proteins are important molecules acting like buffers to modulate dynamics of cytosolic Ca²⁺ transients [13]. Such intracellular proteins can have significant functional consequences on the

Corticothalamic and thalamocortical inputs

The TRN receives monosynaptic glutamatergic inputs mainly from both the cerebral cortex [26], [69], [75] and the thalamus [76], [125]. The only source of CT inputs is layer VI [22], [73]. The CT and TC inputs are recognized as being mainly excitatory [2], [66], [83], [157], [179]. They are topographically organized, with some exceptions, particularly where inputs from higher-order structures are concerned (reviewed by Crabtree [51] and by Guillery et al. [94]). Also, TRN sectors receive

Other afferents

In addition to the cortical and thalamic glutamatergic afferents, the TRN also receives GABAergic [11], [58], [79], [190], cholinergic and monoaminergic inputs [10], [56], [96], [108], [136], [275], most of these being involved in the control of vigilance. Some functional aspects of these modulatory inputs are available elsewhere [156].

Parallel and divergent axonal projections

Ramon y Cajal [212] observed in Golgi impregnated pieces of brain tissue that TRN axons took a ventro-caudal direction, which to all appearances was not the way toward the cerebral cortex. Using similar histological techniques, Scheibel and Scheibel [225] confirmed that TRN axons project to thalamic nuclei (see also Ref. [160]). The principal axon of TRN cells emerges from the soma or a dendrite and usually penetrates the thalamus perpendicularly to the thalamus–TRN interface (see Fig. 3A–C).

Closed- and open-loop thalamo-reticulo-thalamic circuits

It is usually argued that the thalamus and the TRN are reciprocally connected [95], [118], [230]. The reciprocal thalamus-TRN relationship does not, however, fully apply at the cellular level when examining both the anterogradely and the retrogradely labelled neuronal elements following juxtacellular applications of a compound containing biotin [200] (also see Fig. 10). Furthermore, an anatomical study aimed at labelling both afferent and efferent axonal projections from cat TRN loci showed

Large-scale thalamo-reticulo-thalamic circuits

It is generally thought that, unlike to cortical areas, TC neurons do not interact with each other. Crabtree et al. [52], [54] have demonstrated recently in thalamic slices of young rats that glutamate-induced activation of neurons in a thalamic nucleus is associated with inhibition of cellular activities in another distinct but functionally related thalamic nucleus, and conversely. The inhibition is mediated through activation of GABA_A receptors. Because the thalamic slices were free of

Intrinsic cell–cell communications

Various anatomical and functional studies have attempted to show that TRN cells communicate synaptically between each other through dendrodendritic and/or axodendritic synapses. Mutual inhibitory synaptic interactions between TRN cells in the visual sector were first recorded in anaesthetized adult cats [3]. Indeed, electrical stimulation of the optic tract induced a short-latency excitation in TRN cells followed by an inhibitory period, during which the excitatory response that followed

Cellular electrophysiological properties

Reticular cells are endowed with a set of at least 6 voltage-dependent ionic conductances: two classical for Na⁺ and K⁺, a non-inactivated for Na⁺, a low-threshold for Ca²⁺, a Ca²⁺-dependent for K⁺ and a Ca²⁺-dependent non-selective cation current [12], [14], [176], [243]. Low-threshold Ca²⁺ conductance is well known to underlay high-frequency bursts of up to 15 action potentials (200–500 Hz) with an acceleration-deceleration pattern [12], [41]. This transient Ca²⁺ conductance, which might be

Thalamocortical oscillations

At the end of the 19th century, Richard Caton [34] discovered that the brain is an extraordinary machine producing spontaneous electrical waves. Hans Berger [20] characterized the human alpha oscillations, which were modified by activation of sensory systems. He believed that electrocortical rhythms were intracortically generated (also see [115], [214]). Since then several other rhythms have been recorded in association with the wake–sleep cycle, with cognitive tasks and/or with clinical

An ideal substrate for selective attention?

That the TRN is involved in attentional processes is supported by recent findings. McAlonan and Brown [155] revealed that a given attended conditioned sensory stimulus induces in the corresponding TRN sector a significant increase of the number of neurons immunoreactive to the Fos protein. The involvement of the TRN in cognition is highlighted further following directly and indirectly induced neuronal lesions. Lesions of TRN regions usually induce forms of behavioural neglect, suggesting that

Concluding comments

The TRN is a diencephalic GABAergic nucleus, which is composed of neuronal elements endowed with diverse architectural, functional, neurochemical and pharmacological properties. Thus, it might be reasonable to define a TRN cellular type on the basis of its morphological, anatomical, neurochemical and physiological properties.

Nowadays, with single-cell electrophysiological studies conducted in in vitro and in vivo preparations great strides have been made in the understanding of certain

Acknowledgements

This manuscript was prepared with the financial support of the French Institute of Health and Medical Research (INSERM). I would like to thank Laszlo Acsady, Martin Deschênes, Ray Guillery, Anita Lüthi, Yoland Smith and the anonymous referees for their constructive suggestions and comments.

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ReviewThe thalamic reticular nucleus: structure, function and concept

Abstract

Section snippets

Virtually all functional modalities

Receptive field properties

Diverse somatodendritic architectures

Cellular neurochemical diversities

Corticothalamic and thalamocortical inputs

Other afferents

Parallel and divergent axonal projections

Closed- and open-loop thalamo-reticulo-thalamic circuits

Large-scale thalamo-reticulo-thalamic circuits

Intrinsic cell–cell communications

Cellular electrophysiological properties

Thalamocortical oscillations

An ideal substrate for selective attention?

Concluding comments

Acknowledgements

Brain Res.

Brain Res.

Trends Neurosci.

Exp. Neurol.

Conscious. Cogn.

Dev. Brain Res.

Brain Res.

Neuroscience

Electroencephalogr. Clin. Neurophysiol.

Brain Res.

J. Chem. Neuroanat.

Neuroscience

Neurosci. Lett.

Brain Res.

Brain Res.

Neuroscience

Exp. Neurol.

Neuroscience

Dev. Brain Res.

Neurosci. Lett.

Brain Res. Bull.

Trends Neurosci.

J. Chem. Neuroanat.

Brain Res. Bull.

Neuroscience

Neuron.

Trends Neurosci.

The Berger Rhythm: potential changes from occipital lobes in man

Brain

Convergent thalamic and cortical projections—the non-specific system

GABA-mediated biphasic inhibitory responses in hippocampus

Nature

Physiological basis of the alpha rhythm

Inhibitory phasing of neuronal discharge

Nature

Thalamo-cortical processing of vibrissal information in the rat: II. Spatiotemporal convergence in the thalamic ventroposterior medial nucleus (VPm) and its relevance to generation of receptive fields of S1 cortical “barrel” neurones

J. Comp. Neurol.

Bemerkungen uber den Bau des Hirns und Ruchenmarks nebst Beitragen zur Physiologie des zehnten und elften Hirnnerven, mehren kritischen Mittheilungen sowei verschiedenen pathologischen und anatomischen

Noradrenergic innervation of the thalamic reticular nucleus: a light and electron microscopic immunohistochemical study in rats

J. Comp. Neurol.

GABAergic and pallidal terminals in the thalamic reticular nucleus of squirrel monkeys

Exp. Brain Res.

Intrinsic properties of nucleus reticularis thalami neurones of the rat studied in vitro

J. Physiol. (Lond)

Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker

J. Physiol. (Lond)

Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro

J. Physiol. (Lond)

A reticuloreticular commissural pathway in the rat thalamus

J. Comp. Neurol.

Uber das Elektrenkephalogramm des Menschen

Arch. Psychiatr.

Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer

Eur. J. Neurosci.

Cerveau isolé et physiologie du sommeil

C. R. Soc. Biol. Paris

Depolarization of neurones in the isolated olfactory cortex of the guinea-pig by gamma-aminobutyric acid

Br. J. Pharmacol.

Heterogeneity of cell firing properties and opioid sensitivity in the thalamic reticular nucleus

Neuroscience

Differential effect of functional ablation of thalamic reticular nucleus on the acquisition of passive and active avoidance

Int. J. Neurosci.

Review
The thalamic reticular nucleus: structure, function and concept