Cumulative latency advance underlies fast visual processing in desynchronized brain state

Abstract

Fast sensory processing is vital for the animal to efficiently respond to the changing environment. This is usually achieved when the animal is vigilant, as reflected by cortical desynchronization. However, the neural substrate for such fast processing remains unclear. Here, we report that neurons in rat primary visual cortex (V1) exhibited shorter response latency in the desynchronized state than in the synchronized state. In vivo whole-cell recording from the same V1 neurons undergoing the two states showed that both the resting and visually evoked conductances were higher in the desynchronized state. Such conductance increases of single V1 neurons shorten the response latency by elevating the membrane potential closer to the firing threshold and reducing the membrane time constant, but the effects only account for a small fraction of the observed latency advance. Simultaneous recordings in lateral geniculate nucleus (LGN) and V1 revealed that LGN neurons also exhibited latency advance, with a degree smaller than that of V1 neurons. Furthermore, latency advance in V1 increased across successive cortical layers. Thus, latency advance accumulates along various stages of the visual pathway, likely due to a global increase of membrane conductance in the desynchronized state. This cumulative effect may lead to a dramatic shortening of response latency for neurons in higher visual cortex and play a critical role in fast processing for vigilant animals.state-dependent temporal processing | synaptic inputs | hierarchical accumulation F ast reaction is essential for the survival of animals, such as when detecting and fleeing a predator. Humans or animals react rapidly in a vigilant state (1-3). The vigilance level of animals (also humans) varies with brain state, which can be characterized by the patterns of population activities measured by electroencephalogram (EEG) and local field potential (LFP) (4, 5). Although brain state exhibits diverse activity patterns, it can be broadly classified into a desynchronized state dominated by small-amplitude, high-frequency activities, and a synchronized state dominated by large-amplitude, low-frequency fluctuations (4, 5). The brain operates in the desynchronized state when the animal is alert or vigilant, whereas it operates in the synchronized state when the animal is quiescent or drowsy (4, 5). To understand the neural substrate for fast processing in the vigilant state, it is important to compare response latencies in the two brain states for sensory cortical neurons, which are at the initial stage along the sensorimotor pathway.Brain state has a dominant impact on both resting properties (6, 7) and sensory evoked responses (4, 8, 9) of cortical neurons. For the visual system, although brain state or behavioral state can modulate response amplitude, spatial receptive field, and temporal frequency tuning of the neurons in the early visual pathway (10-13), it is not clear whether brain state can modulate response latency of primary visual cortex (V1) neurons. Furthermore, the ...

Visual response properties of neurons in the superficial layers of the superior colliculus of awake mouse

“…; Wang et al . ). One intriguing possibility is that anaesthesia may also have strong impact on recurrent networks in the sSC that are probably important in building response properties.…”

“…); these may be reduced by anaesthesia (Wang et al . ). Similarly, intracollicular inhibitory connections are probably important in shaping functional tuning (Inayat et al .…”

“…We do not know the origin of the functional differences that we see between awake and anaesthetized animals because there are several potential mechanisms mediating the effect of anaesthesia on the spontaneous and evoked firing rate (Sceniak & Maciver, 2006;Haider et al 2013;Wang et al 2014). One intriguing possibility is that anaesthesia may also have strong impact on recurrent networks in the sSC that are probably important in building response properties.…”

“…One intriguing possibility is that anaesthesia may also have strong impact on recurrent networks in the sSC that are probably important in building response properties. For example, direction tuned neurons in the sSC receive directionally tuned input from the retina that is amplified by intracollicular excitatory connections between neurons with similar directional preferences (Shi et al 2017); these may be reduced by anaesthesia (Wang et al 2014). Similarly, intracollicular inhibitory connections are probably important in shaping functional tuning (Inayat et al 2015) and anaesthesia-dependent changes in inhibition may be important, as in the primary visual cortex (Haider et al 2013).…”

Population Responses in V1 Encode Different Figures by Response Amplitude

“…This was done for each recording session separately [on the mean measure smoothed with a Gaussian filter with a width (2) of 40 ms]. The second derivative could efficiently capture the beginning of the sharp increase of the ⌬FF measure (Boudreau and Ferster, 2005;Meeks and Mennerick, 2007;Wang et al, 2014;Fig. 4E).…”