Morphological Correlates of Triadic Circuitry in the Lateral Geniculate Nucleus of Cats and Rats

Abstract

. We used an in vitro slice preparation of the lateral geniculate nucleus in cats and rats to study morphological correlates of triadic circuitry in relay cells. The three triadic elements involve a retinal synapse onto a GABAergic dendritic terminal of an interneuron, a synapse from the same retinal terminal onto a relay cell dendrite, and a synapse from the same interneuron terminal onto the same relay cell dendrite. We made whole cell recordings and labeled cells with biocytin. Previous methods were used to identify triadic circuitry based on evidence that the retinal terminal activates a metabotropic glutamate receptor on the interneuronal terminal. Thus application of (Ϯ)-1-aminocyclopentane-trans-1,3-dicarboxylic acid (an agonist to that receptor) increases the rate of spontaneous inhibitory postsynaptic currents (sIPSCs) recorded in the relay cell, and if some of this increase remains with further addition of TTX (a TTX-insensitive response), a triad is indicated. We quantified the extent of the TTX-insensitive response and sought morphological correlates. In both rats and cats, this response correlated (negatively) with the number of primary dendrites and (positively) with polarity of the dendritic arbor. There was no correlation with cell size. Curiously, in cats, this response correlated with the presence of appendages at primary dendritic branches, but there was no such correlation in rats. These observations in cats map onto the X/Y classification, with X cells having triads, but it is not clear from our results if a comparable classification exists for rats. I N T R O D U C T I O NA ubiquitous feature of thalamic circuitry is a triadic synaptic arrangement that involves many of the inputs carrying information to be relayed to cortex (reviewed in Sherman and Guillery 1996). It is called "triadic," because three synapses are involved (see Fig. 1). The clearest and most thoroughly studied example involves retinal input to the lateral geniculate nucleus in the cat. Here, a glutamatergic retinal terminal contacts both a relay cell dendrite as well as a synaptic terminal from a GABAergic interneuron, and the dendritic terminal contacts the same relay cell dendrite. These dendritic terminals are the only ones in thalamus that are both pre-and postsynaptic. In the A layers of the cat's lateral geniculate nucleus, many retinal terminals are involved in such triads, and this is a signature of the X cell pathway (reviewed in Sherman and Guillery 1996, 2004a,b); other retinal terminals contact relay cell dendrites in simple synapses without involvement of terminals from dendrites of interneurons, and this is typical of the Y cell pathway.However, the distinction is not absolute because a small minority of retinal inputs to X cells is nontriadic, ending in simple contacts onto a relay cell dendrite, and vice versa for Y cells.In an attempt to begin to unravel the function of the triad in the cat's lateral geniculate nucleus, we have recently confirmed previous immunocytochemical evidence ( Godwin et al. 1996) t...

Synaptic Release Generates a Tonic GABAAReceptor-Mediated Conductance That Modulates Burst Precision in Thalamic Relay Neurons

“…As shown in Figure 1C, in dLGN, putative relay neurons were observed with both X-and Y-like properties. X-like neurons had a polar distribution of primary dendrites with obvious spines, compared with the radial distribution of smooth dendrites reported for Y-like neurons (Sherman and Guillery, 1996;Lam et al, 2005). No obvious Y-like morphology has thus far been encountered in the vLGN, and interneuron-like morphology was only observed for one recovered cell in both the dLGN and vLGN data sets.…”

GABAAReceptor-Mediated Tonic Inhibition in Thalamic Neurons

“…cate that there is no difference in tonic inhibition among potential TC neuron subclasses, for instance in the dLGN (Lam et al, 2005). We also suggest that, because in all likelihood the concentration of ambient GABA in our slices under control conditions is lower than that which exists in vivo (Lerma et al, 1986), our apparent tonic current amplitude in vitro may be an underestimation of its in vivo counterpart.…”

“…Second, the low GBZ concentration incompletely penetrates the synapse and/or is outcompeted by the high concentration of vesicularly released GABA in the synapse, resulting in only partial receptor blockade and maintenance of phasic inhibition. This second factor may be further compounded by the existence of synaptic glomeruli, complex triadic synaptic arrangements surrounded by glial sheaths, on some if not all TC neurons in the rat dLGN (Ohara et al, 1983;Lam et al, 2005). However, we stress that the subcellular distribution of extrasynaptic receptors in the thalamus is unknown.…”

Mapping by Laser Photostimulation of Connections Between the Thalamic Reticular and Ventral Posterior Lateral Nuclei in the Rat

“…Whole cell recordings were performed using a visualized slice preparation as described previously (Lam et al 2005). Recording pipettes were pulled from borosilicate glass capillaries and had tip resistances of 4 -8 M⍀ when filled with the appropriate solution.…”