Functional Organization of the Thalamic Input to the Thalamic Reticular Nucleus

Abstract

Most axons connecting the thalamus and cortex in both directions pass through the thalamic reticular nucleus (TRN), a thin layer of GABAergic cells adjacent to the thalamus, and innervate neurons there. The TRN, therefore, is in a strategic location to regulate thalamocortical communication. We recorded from neurons of the somatosensory region of the TRN in a thalamocortical slice preparation and studied the spatial organization of their thalamic input using laser scanning photostimulation. We show that the thalamoreticular pathway is organized topographically for most neurons. The somatosensory region of the TRN can be organized into three tiers. From the inner (thalamoreticular) border to the outer, in a manner roughly reciprocal to the reticulothalamic pathway, each of these tiers receives its input from one of the somatosensory relays of the thalamus, POm, VPM and VPL, respectively. What is surprising is that about a quarter of the recorded neurons received input from multiple thalamic regions usually located in different nuclei. These neurons distribute quite evenly throughout the thickness of the TRN. Our results, therefore, suggest that there exist a subpopulation of TRN neurons that receive convergent inputs from multiple thalamic sources and engage in more complex patterns of inhibition of relay cells. We propose these neurons enable the TRN to act as an externally driven “searchlight” that integrates cortical and subcortical inputs and then inhibits or disinhibits specific thalamic relay cells, so that appropriate information can get through the thalamus to the cortex.

The calcium-binding protein parvalbumin modulates the firing 1 properties of the reticular thalamic nucleus bursting neurons

“…Moreover, the synaptic strength of the corticothalamic collaterals is much weaker than the synaptic strength of the thalamocortical collaterals (Liu et al 2001). In light of our results we suggest that the positive cross-correlograms showing synchronized activity are the result of the thalamocortical collaterals to the RTN (Villa et al 1999;Lam and Sherman 2011). Thus, in the absence of PV, the functional connectivity of RTN during spontaneous activity would remain unaffected.…”

“…Our current knowledge of the RTN indicates that the connections are not the same for each sector (Guillery et al 1998;Lam and Sherman 2011) and we do not exclude that the RTN firing types of the rostral sector of the nucleus may have a spatial organization, but a detailed and evenly distributed sample of recording sites should be collected to answer this question. Our study suggests that different firing types are present in the RTN; it remains to be understood whether these are biologically patterned or whether the same cellular type could fire in different modes according to different arousal or attentive states.…”

“…It is worth mentioning that our recordings were performed in vivo in the anterior tier of the RTN (approximately corresponding to the limbic and somatosensory portion of the nucleus; Jones 1975Jones , 1991, whereas the studies that defined a spatial organization of neurons with different firing properties within the RTN were performed in the somatosensory sector of the rat (Lee et al 2007) and mouse slices (Lam and Sherman 2011) and in the cat dorsolateral sector (corresponding to the auditory sector, Villa 1990). Notice that the RTN is abundantly innervated by cholinergic fibers that may contribute to modulate the firing properties of its neurons in vivo (Jones 1991;Villa et al 1996).…”

“…Recent findings have shown that these collateral synapses within RTN are likely to be much weaker than the RTN-TC synapses (Lam et al 2006). Despite the observation of gap junctions between RTN neurons (Landisman et al 2002), their ability to propagate the activity over the nucleus is likely to be less important than the dominant form of reticulo-reticular connectivity driven by axodendritic synapses (Lam et al 2006). Therefore, the intra-RTN connections are likely to contribute marginally to synchronization of cell pairs during spontaneous activity.…”

Lateral thalamic control of nociceptive response after whisker pad injection of varicella zoster virus

“…Interestingly, all neurons in the reticular thalamic region express GABA with only a miniscule population of GABA positive cells in the adjacent ventroposterior nuclei (Barbaresi et al, 1986). Neurons in the ventroposterior thalamic nucleus send collaterals to the adjacent reticular thalamic nucleus and GABA positive neurons in the reticular thalamic nucleus send axons back to the ventroposterior thalamic nucleus “gating” pain signals passing through the thalamus to the cortex (Vahle-Hinz et al, 1994; Lam and Sherman, 2011). The trigeminal nuclei project to the posterior thalamic nucleus and GABA neurons in the zona incerta affect thalamic activity (Masri et al, 2009; Chang et al, 2012).…”