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Inhibitory projections from the visual sector of the thalamic reticular nucleus to the lateral geniculate nucleus complete the earliest feedback loop in the mammalian visual pathway and regulate the flow of information from retina to cortex. There are two competing hypotheses about the function of the thalamic reticular nucleus. One regards the structure as a thermostat that uniformly regulates thalamic activity through negative feedback. Alternatively, the searchlight hypothesis argues for a role in focal attentional modulation through positive feedback, consistent with observations that behavioral state influences reticular activity. Here, we address the question of whether cells in the reticular nucleus have receptive fields small enough to provide localized feedback by devising methods to quantify the size of these fields across visual space. Our results show that reticular neurons in the cat operate over discrete spatial scales, at once supporting the searchlight hypothesis and a role in feature selective sensory processing.The searchlight hypothesis proposes that the thalamic reticular nucleus regulates thalamic relay activity through focal attentional modulation. Here the authors show that the receptive field sizes of reticular neurons are small enough to provide localized feedback onto thalamic neurons in the visual pathway.

All visual signals the cortex receives are influenced by the perigeniculate sector (PGN) of the thalamic reticular nucleus, which receives input from relay cells in the lateral geniculate and provides feedback inhibition in return. Relay cells have been studied in quantitative depth; they behave in a roughly linear fashion and have receptive fields with a stereotyped center-surround structure. We know far less about reticular neurons. Qualitative studies indicate they simply pool ascending input to generate non-selective gain control. Yet the perigeniculate is complicated; local cells are densely interconnected and fire lengthy bursts. Thus, we employed quantitative methods to explore the perigeniculate using relay cells as controls. By adapting methods of spike-triggered averaging and covariance analysis for bursts, we identified both first and second order features that build reticular receptive fields. The shapes of these spatiotemporal subunits varied widely; no stereotyped pattern emerged. Companion experiments showed that the shape of the first but not second order features could be explained by the overlap of On and Off inputs to a given cell. Moreover, we assessed the predictive power of the receptive field and how much information each component subunit conveyed. Linear-non-linear (LN) models including multiple subunits performed better than those made with just one; further each subunit encoded different visual information. Model performance for reticular cells was always lesser than for relay cells, however, indicating that reticular cells process inputs non-linearly. All told, our results suggest that the perigeniculate encodes diverse visual features to selectively modulate activity transmitted downstream.

Synapses made by local interneurons dominate the thalamic circuits that process signals traveling from the eye downstream. The anatomical and physiological differences between interneurons and the (relay) cells that project to cortex are vast. To explore how these differences might influence visual processing, we made intracellular recordings from both classes of cells in vivo in cats. Macroscopically, all receptive fields were similar, consisting of two concentrically arranged subregions in which dark and bright stimuli elicited responses of the reverse sign. Microscopically, however, the responses of the two types of cells had opposite profiles. Excitatory stimuli drove trains of single excitatory postsynaptic potentials in relay cells, but graded depolarizations in interneurons. Conversely, suppressive stimuli evoked smooth hyperpolarizations in relay cells and unitary inhibitory postsynaptic potentials in interneurons. Computational analyses suggested that these complementary patterns of response help to preserve information encoded in the fine timing of retinal spikes and to increase the amount of information transmitted to cortex.

Thalamic relay cells fire action potentials that transmit information from retina to cortex. The amount of information that spike trains encode is usually estimated from the precision of spike timing with respect to the stimulus. Sensory input, however, is only one factor that influences neural activity. For example, intrinsic dynamics, such as oscillations of networks of neurons, also modulate firing pattern. Here, we asked if retinal oscillations might help to convey information to neurons downstream. Specifically, we made whole-cell recordings from relay cells to reveal retinal inputs (EPSPs) and thalamic outputs (spikes) and then analyzed these events with information theory. Our results show that thalamic spike trains operate as two multiplexed channels. One channel, which occupies a low frequency band (<30 Hz), is encoded by average firing rate with respect to the stimulus and carries information about local changes in the visual field over time. The other operates in the gamma frequency band (40-80 Hz) and is encoded by spike timing relative to retinal oscillations. At times, the second channel conveyed even more information than the first. Because retinal oscillations involve extensive networks of ganglion cells, it is likely that the second channel transmits information about global features of the visual scene.

Thalamic relay cells transmit information from retina to cortex by firing either rapid bursts or tonic trains of spikes. Bursts occur when the membrane voltage is low, as during sleep, because they depend on channels that cannot respond to excitatory input unless they are primed by strong hyperpolarization. Cells fire tonically when depolarized, as during waking. Thus, mode of firing is usually associated with behavioral state. Growing evidence, however, suggests that sensory processing involves both burst and tonic spikes. To ask if visually evoked synaptic responses induce each type of firing, we recorded intracellular responses to natural movies from relay cells and developed methods to map the receptive fields of the excitation and inhibition that the images evoked. In addition to tonic spikes, the movies routinely elicited lasting inhibition from the center of the receptive field that permitted bursts to fire. Therefore, naturally evoked patterns of synaptic input engage dual modes of firing.