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Some cortical neurons receive highly selective thalamocortical (TC) input, but others do not. Here, we examine connectivity of single thalamic neurons (lateral geniculate nucleus, LGN) onto putative fast-spike inhibitory interneurons in layer 4 of rabbit visual cortex. We show that three ‘rules’ regulate this connectivity. These rules concern: (1) the precision of retinotopic alignment, (2) the amplitude of the postsynaptic local field potential elicited near the interneuron by spikes of the LGN neuron, and (3) the interneuron’s response latency to strong, synchronous LGN input. We found that virtually all first-order fast-spike interneurons receive input from nearly all LGN axons that synapse nearby, regardless of their visual response properties. This was not the case for neighboring regular-spiking neurons. We conclude that profuse and highly promiscuous TC inputs to layer-4 fast-spike inhibitory interneurons generate response properties that are well-suited to mediate a fast, sensitive, and broadly tuned feed-forward inhibition of visual cortical excitatory neurons.

Awake mammals can switch between alert and nonalert brain states hundreds of times per day. Here, we study the effects of alertness on two cell classes in layer 4 of primary visual cortex of awake rabbits: presumptive excitatory "simple" cells and presumptive fast-spike inhibitory neurons (suspected inhibitory interneurons). We show that in both cell classes, alertness increases the strength and greatly enhances the reliability of visual responses. In simple cells, alertness also increases the temporal frequency bandwidth, but preserves contrast sensitivity, orientation tuning, and selectivity for direction and spatial frequency. Finally, alertness selectively suppresses the simple cell responses to high-contrast stimuli and stimuli moving orthogonal to the preferred direction, effectively enhancing mid-contrast borders. Using a population coding model, we show that these effects of alertness in simple cells-enhanced reliability, higher gain, and increased suppression in orthogonal orientation-could play a major role at increasing the speed of cortical feature detection.

Sensory adaptation serves to adjust awake brains to changing environments on different time scales. However, adaptation has been studied traditionally under anesthesia and for short time periods. Here, we demonstrate in awake rabbits a novel type of sensory adaptation that persists for Ͼ1 h and acts on visual thalamocortical neurons and their synapses in the input layers of the visual cortex. Following prolonged visual stimulation (10 -30 min), cells in the dorsal lateral geniculate nucleus (LGN) show a severe and prolonged reduction in spontaneous firing rate. This effect is bidirectional, and prolonged visually induced response suppression is followed by a prolonged increase in spontaneous activity. The reduction in thalamic spontaneous activity following prolonged visual activation is accompanied by increases in 1) response reliability, 2) signal detectability, and 3) the ratio of visual signal/spontaneous activity. In addition, following such prolonged activation of an LGN neuron, the monosynaptic currents generated by thalamic impulses in layer 4 of the primary visual cortex are enhanced. These results demonstrate that in awake brains, prolonged sensory stimulation can have a profound, long-lasting effect on the information conveyed by thalamocortical inputs to the visual cortex. lateral geniculate nucleus; thalamocortical; sensory adaptation THE VISUAL SYSTEM IS HIGHLY dynamic, able to scale neuronal responses across several orders of magnitude of mean luminance and to alter tuning specificity based on recent visual experience. Adaptations of neural responses, lasting from seconds (Baccus and Meister 2002;Brown and Masland 2001;Rieke 2001) to minutes (Dragoi et al. 2000;Giaschi et al. 1993;Hammond et al. 1988;McLelland et al. 2009;Ohzawa et al. 1985;Vautin and Berkley 1977), have been described, with the longest lasting adaption ϳ10 min (Dragoi et al. 2000). Yet, the perceptual effects of long-duration adapting stimuli can last considerably longer [see, for example, Dong et al. (2014) Here, we describe a novel form of adaptation, following prolonged visual stimulation, in which the spontaneous activity of neurons in the lateral geniculate nucleus (LGN) of awake rabbits is reduced to as little as 10% of pre-adaptation baseline activity levels and slowly recovers over a period of Ͼ1 h. We demonstrate that this adaptation, which is cell specific and retinotopically precise, is accompanied by an increase in the reliability (reduced Fano factor) and detectability [increased area of receiver operator characteristic (ROC) functions] of visual responses and by an increase in the ratio of evoked-tospontaneous firing rates. We also show that during the adapted period, monosynaptic currents, generated in layer 4 by thalamic impulses, are greatly increased, providing a mechanism for further enhancing the saliency of visual stimuli. Finally, we show that visual stimuli that suppress cell responses for a prolonged period of time can have the opposite effect and generate a prolonged increase in thalamic spontaneous activ...

Directionally selective (DS) neurons are found in the retina and lateral geniculate nucleus (LGN) of rabbits and rodents, and in rabbits, LGN DS cells project to primary visual cortex. Here, we compare visual response properties of LGN DS neurons with those of layer 4 simple cells, most of which show strong direction/orientation selectivity. These populations differed dramatically, suggesting that DS cells may not contribute significantly to the synthesis of simple receptive fields: 1) whereas the first harmonic component (F1)-to-mean firing rate (F0) ratios of LGN DS cells are strongly nonlinear, those of simple cells are strongly linear; 2) whereas LGN DS cells have overlapped ON/OFF subfields, simple cells have either a single ON or OFF subfield or two spatially separate subfields; and 3) whereas the preferred directions of LGN DS cells are closely tied to the four cardinal directions, the directional preferences of simple cells are more evenly distributed. We further show that directional selectivity in LGN DS neurons is strongly enhanced by alertness via two mechanisms, 1) an increase in responses to stimulation in the preferred direction, and 2) an enhanced suppression of responses to stimuli moving in the null direction. Finally, our simulations show that these two consequences of alertness could each serve, in a vector-based population code, to hasten the computation of stimulus direction when rabbits become alert.

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