Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus

Abstract

Detailed information regarding the contribution of individual ␥-aminobutyric acid (GABA)-containing inhibitory neurons to the overall synaptic activity of single postsynaptic cells is essential to our understanding of fundamental elements of synaptic integration and operation of neuronal circuits. For example, GABA-containing cells in the thalamic reticular nucleus (nRt) provide major inhibitory innervation of thalamic relay nuclei that is critical to thalamocortical rhythm generation. To investigate the contribution of individual nRt neurons to the strength of this internuclear inhibition, we obtained whole-cell recordings of unitary inhibitory postsynaptic currents (IPSCs) evoked in ventrobasal thalamocortical (VB) neurons by stimulation of single nRt cells in rat thalamic slices, in conjunction with intracellular biocytin labeling. Two types of monosynaptic IPSCs could be distinguished. ''Weak'' inhibitory connections were characterized by a significant number of postsynaptic failures in response to presynaptic nRt action potentials and relatively small IPSCs. In contrast, ''strong'' inhibition was characterized by the absence of postsynaptic failures and significantly larger unitary IPSCs. By using miniature IPSC amplitudes to infer quantal size, we estimated that unitary IPSCs associated with weak inhibition resulted from activation of 1-3 release sites, whereas stronger inhibition would require simultaneous activation of 5-70 release sites. The inhibitory strengths were positively correlated with the density of axonal swellings of the presynaptic nRt neurons, an indicator that characterizes different nRt axonal arborization patterns. These results demonstrate that there is a heterogeneity of inhibitory interactions between nRt and VB neurons, and that variations in gross morphological features of axonal arbors in the central nervous system can be associated with significant differences in postsynaptic response characteristics.Intrathalamic rhythmic activities that are prominent in sleep and certain pathophysiological conditions (reviewed in ref. 1) are a consequence of both the intrinsic properties of thalamic neurons and the reciprocal synaptic connectivity between excitatory cells in thalamic relay nuclei and inhibitory neurons in the thalamic reticular nucleus (nRt) (or analogous perigeniculate nucleus) (2-5). Most thalamic neurons are capable of firing action potentials in robust phasic bursts that are key elements in rhythm generation. Burst behavior, in turn, depends on the presence of a low-threshold transient Ca 2ϩ current (6, 7) that is inactivated at resting membrane potentials and deinactivated by inhibitory postsynaptic potentials that hyperpolarize the involved neurons (2, 3, 8). The ␥-aminobutyric acid (GABA)-ergic inhibitory innervation onto thalamocortical relay neurons from nRt (3, 9-13) thus forms a key element in the generation of oscillatory activities.In this scheme of thalamic operation, it becomes critical to define the factors that regulate the inhibitory drive from nRt neur...

Attentional Modulation of Thalamic Reticular Neurons

“…Both of these inputs to TRN are excitatory. In striking contrast, the projections from TRN back on the LGN are inhibitory (Cox et al, 1997;Kim et al, 1997).…”

The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity

“…0.03 mS, and increased to 0.2 mS under in vivo conditions. For an estimated quantal conductance of GABA A synapses of 300 pS (Cox et al 1997;Le Feuvre et al 1997;Ulrich & Huguenard 1997), the threshold conductances predict that between 100 (control) and 660 (in vivo) GABAergic synapses must be co-activated to elicit a rebound burst in thalamic relay cells. Morphological studies indicate that a single axon from reticular neurons establish, on average, 60 synapses on the same postsynaptic relay cell (Kim et al 1997).…”

Early Development of the Thalamic Inhibitory Feedback Loop in the Primary Somatosensory System of the Newborn Mice

“…It has also been shown that the amplitude of unitary nRT-to-nVPM IPSCs of older rats (P9 -P16) varied widely from 18 to 514 pA (Cox et al, 1997). However, there is no systematic study of the nRT-to-nVPM IPSCs during the first postnatal week; therefore, we studied the changes with age of the GABA A -mediated nRTto-nVPM IPSCs from P0 to P9 (Table 1, Fig.…”