Encoding of visual information by LGN bursts. Thalamic relay cells respond to visual stimuli either in burst mode, as a result of activation of a low-threshold Ca2+ conductance, or in tonic mode, when this conductance is inactive. We investigated the role of these two response modes for the encoding of the time course of dynamic visual stimuli, based on extracellular recordings of 35 relay cells from the lateral geniculate nucleus of anesthetized cats. We presented a spatially optimized visual stimulus whose contrast fluctuated randomly in time with frequencies of up to 32 Hz. We estimated the visual information in the neural responses using a linear stimulus reconstruction method. Both burst and tonic spikes carried information about stimulus contrast, exceeding one bit per action potential for the highest variance stimuli. The "meaning" of an action potential, i.e., the optimal estimate of the stimulus at times preceding a spike, was similar for burst and tonic spikes. In within-trial comparisons, tonic spikes carried about twice as much information per action potential as bursts, but bursts as unitary events encoded about three times more information per event than tonic spikes. The coding efficiency of a neuron for a particular stimulus is defined as the fraction of the neural coding capacity that carries stimulus information. Based on a lower bound estimate of coding efficiency, bursts had approximately 1.5-fold higher efficiency than tonic spikes, or 3-fold if bursts were considered unitary events. Our main conclusion is that both bursts and tonic spikes encode stimulus information efficiently, which rules out the hypothesis that bursts are nonvisual responses.

Glutamate has an important neuromodulatory role in synaptic transmission through metabotropic glutamate receptors (mGluRs) linked to a variety of G-protein-coupled second messenger pathways. Activation of these receptors on relay cells in the lateral geniculate nucleus (LGN) with the agonist trans-(1S,3R)-1-amino-1, 3-cyclopentanedicarboxylic acid produces a membrane depolarization that inactivates the low-threshold Ca2+ spike, causing a transition from burst to tonic response mode. The excitatory effects of metabotropic receptor activation in the LGN appear to be produced through the receptors linked to phosphoinositide hydrolysis and apparently only through activation of the corticogeniculate pathway. Two mGluRs, mGluR1alpha (a splice variant of mGluR1) and mGluR5, are linked to the phosphoinositide system. We examined the localization of these receptors with affinity-purified, anti-peptide, polyclonal antibodies raised to the C-terminal region of each receptor protein. Under examination with the light microscope, we found that both types of receptors are present in the geniculate neuropil and in that of the overlying thalamic reticular nucleus, including the perigeniculate nucleus. We also examined the ultrastructural localization of immunolabel with the electron microscope, using a postembedding immunogold marker to identify terminals, dendrites, and somata that contain GABA. Label for the antibody directed against mGluR1alpha was primarily localized in the dendrites of relay cells, postsynaptic to various terminal types. Of these, terminal profiles normally associated with corticogeniculate inputs predominated, whereas retinal terminal profiles were scarce. Label for the antibody directed against mGluR5 label was prominent in inhibitory F2-terminal profiles associated with the retinal input to relay cells. In the perigeniculate nucleus, both mGluRs were localized to dendrites. The distribution of the two phosphoinositide-linked mGluRs in the LGN suggests very different functional roles for the two receptor types. We conclude from these data that mGluR1 appears to have a dominant role in corticogeniculate control of response mode through the feedback glutamatergic pathway from layer VI, whereas mGluR5 is positioned to affect retinogeniculate activation of relay cells through feed forward glomerular interactions.

We examined neurofilament staining in the normal and visually deprived lateral geniculate nucleus (LGN), using the SMI-32 antibody. This antibody preferentially stains LGN cells that display the morphological characteristics of Y-cells. The soma sizes of SMI-32-stained cells were consistent with those of the overall population of Y-cells, and the Golgi-like staining of their dendrites revealed a radial distribution that often crossed laminar boundaries. Labeled cells were distributed within the A laminae (primarily near laminar borders), the magnocellular portion of the C laminae, and the medial intralaminar nucleus, but they were absent in the parvocellular C laminae. Electron microscopic examination of SMI-32-stained tissue revealed that staining was confined to somata, dendrites, and large myelinated axons. Retinal synapses on SMI-32-labeled dendrites were primarily simple axodendritic contacts; few triadic arrangements were observed. In the LGN of cats reared with monocular lid suture, SMI-32 staining was decreased significantly in the A laminae that received input from the deprived eye. Dephosphorylation of the tissue did not alter the cellular SMI-32 staining patterns. Analysis of staining patterns in the C laminae and monocular zone of the A laminae suggests that changes in the cytoskeleton after lid suture reflect cell class and not binocular competition. Taken together, the results from normal and lid-sutured animals suggest that the cat LGN offers a unique model system in which the cytoskeleton of one class of cells can be manipulated by altering neuronal activity.