Furthermore, selective stimulation of the direct feedback projection modulates V1 activity in mice ( Zhang et al., 2014). Indeed, the neuronal activities of higher-order and low-level visual cortices are synchronized during top-down attention ( von Stein et al., 2000 Engel et al., 2001 Gregoriou et al., 2009) and stimulation of the frontal cortex enhances the activity of the low-level visual region in monkeys ( Moore and Armstrong, 2003). Because of their relationships with cognitive functions, late sensory responses are expected to be generated through feedback inputs from higher-order cortices ( Gilbert and Li, 2013). More recently, the delayed component of the visual response, referred to as a late response, has gained increasing attention in terms of sensory cognition ( Del Cul et al., 2007), sensory attention ( Roelfsema et al., 1998 Reynolds et al., 2000), iconic memory ( Dick, 1974 Benucci et al., 2007), and working memory ( Supèr et al., 2001 Harrison and Tong, 2009 Munneke et al., 2010). Studies have mostly targeted this immediate early response for which the basic properties are well described ( Ohki et al., 2005 Niell and Stryker, 2008 Priebe and Ferster, 2008 Jia et al., 2010 Hofer et al., 2011 Liu et al., 2011). Through this multisynaptic transmission, V1 neurons respond with a short latency after the presentation of a visual stimulus, which is referred to herein as an early response. The primary visual cortex (V1) is where light information, which reaches V1 via the retina and the dorsal lateral geniculate nucleus (dLGN) of the thalamus, classically referred to as the feedforward pathway, first reaches the neocortex ( Felleman and Van Essen, 1991 Purves et al., 2001). In addition, during the late response, excitation and inhibition are balanced, but inhibition is dominant in patterning action potentials. The mechanism of neocortical late responses was investigated using multiple electrophysiological techniques and the findings indicate that it actually arises from the thalamus. SIGNIFICANCE STATEMENT The long-delayed responses of neocortical neurons are thought to arise from cortical feedback activity that is related to sensory perception and cognition. Therefore, the late component of a sensory-evoked cortical response should be interpreted with caution. In contrast to the common assumption that the neocortical late response reflects a feedback signal from the downstream higher-order cortical areas, our pharmacological and optogenetic analyses demonstrated that the late responses likely have a thalamic origin. Using whole-cell patch-clamp recordings, we demonstrated that the late rebound response was shaped by a net-balanced increase in excitatory and inhibitory synaptic conductances, whereas transient imbalances were caused by intermittent inhibitory barrage. In the mouse primary visual cortex in vivo, we isolated long-delayed responses by using a brief light-flash stimulus for which the stimulus late response occurred long after the stimulus offset and was not contaminated by the instantaneous response evoked by the stimulus. However, how the visual late response is generated and organized is not completely understood. The late response is thought to contribute to visual functions such as sensory perception, iconic memory, working memory, and forming connections between temporally separated stimuli. The primary visual cortex exhibits a late, long response with a latency of >300 ms and an immediate early response that occurs ∼100 ms after a visual stimulus.
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