Inhibitory Interactions between Perigeniculate GABAergic Neurons

Abstract

Perigeniculate neurons form an interactive sheet of cells that inhibit one another as well as thalamocortical neurons in the dorsal lateral geniculate nucleus (LGNd). The inhibitory influence of the GABAergic neurons of the perigeniculate nucleus (PGN) onto other PGN neurons was examined with intracellular recordings in vitro. Intracellular recordings from PGN neurons during the generation of spindle waves revealed barrages of EPSPs and IPSPs. The excitation of local regions of the PGN with the local application of glutamate resulted in activation of IPSPs in neighboring PGN neurons. These IPSPs displayed an average reversal potential of Ϫ77 mV and were blocked by application of bicuculline methiodide or picrotoxin, indicating that they are mediated by GABA A receptors. In the presence of GABA A receptor blockade, the activation of PGN neurons with glutamate could result in slow IPSPs that were mediated by GABA B receptors in a subset (40%) of cells. Similarly, application of specific agonists muscimol and baclofen demonstrated that PGN neurons possess both functional GABA A and GABA B receptors. Examination of the axon arbors of biocytin-filled PGN neurons often revealed the presence of beaded axon collaterals within the PGN, suggesting that this may be an anatomical substrate for PGN to PGN inhibition.Functionally, activation of inhibition between PGN neurons could result in a shortening or a complete abolition of the low threshold Ca 2ϩ spike or an inhibition of tonic discharge. We suggest that the mutual inhibition between PGN neurons forms a mechanism by which the excitability of these cells is tightly controlled. The activation of a point within the PGN may result in the inhibition of neighboring PGN neurons. This may be reflected in the LGNd as a center of inhibition surrounded by an annulus of disinhibition, thus forming a "center-surround" mechanism for thalamic function.

Prolonged hyperpolarizing potentials precede spindle oscillations in the thalamic reticular nucleus

“…Because corticothalamic excitatory volleys also could elicit such hyperpolarizations and knowing the propensity of cortex to evoke spindling (12,13,18), we propose that firing in some cortical neuronal pools may excite RE neurons, generating EPSPs and, in some cases, LTSs crowned by spike bursts, which would generate prolonged hyperpolarizations in adjacent and͞or distant RE neurons. There is indeed evidence for both dendrodendritic (10,11) and axoaxonic synapses (42), which mediate inhibitory interactions in the RE nucleus (25,39).…”

“…However, those experiments did not assess a critical point, that is, how much GABA B conductance is activated during thalamic oscillations when large populations of neurons fire in synchrony (13,18). And experiments in ferret slices have shown that GABA B responses to glutamate applied in the perigeniculate sector of the RE nucleus are not so small, as the rebound spike bursts were blocked by an antagonist of GABA B receptors (39). Therefore, the possibility that the RE nucleus expresses a significant GABA B response during spindle oscillations cannot be discarded.…”

Circuits for Multisensory Integration and Attentional Modulation Through the Prefrontal Cortex and the Thalamic Reticular Nucleus in Primates

“…Most neurons have long, sparsely branched, aspiny dendrites, emerging from the poles of the soma, but some have beaded structures along their dendrites / 21 /. The axons of TRN neurons target underlying thalamic nuclei but also send local collaterals within neighboring TRN regions, and interacting through chemical axoaxonic, axosomatic and dendrodendritic synapses inhibit each other / 9,43,82,98,123,146,155,168,175,180 /. Moreover, neighboring reticular neurons in rodents are electrically coupled, forming highly synchronized networks / 28,95 /.…”

Sensorimotor cortical influences on cuneate nucleus rhythmic activity in the anesthetized cat

“…This may indicate that GABA A receptors, known to be abundantly represented in the cuneate, 24,33,55,56 can also induce depolarizing responses. 35,40 It has been repeatedly reported that, upon cortical stimulation, the extracellular firing of cuneate and gracile neurons shows an initial increase followed by a longer period of firing decrease, further followed by a "rebound" facilitation. 11,18 Under our experimental conditions, the cortical excitatory effects on CLs were the fastest observed ( Fig.…”