Inhibition dominates sensory responses in the awake cortex (original) (raw)

In vivo approach to the cellular mechanisms for sensory processing in sleep and wakefulness

Cellular and molecular neurobiology, 2002

1. The present review analyzes sensory processing during sleep and wakefulness from a single neuronal viewpoint. Our premises are that processing changes throughout the sleep-wakefulness cycle may be at least partially evidenced in single neurons by (a) changes in the phase locking of the response to the hippocampal theta rhythm, (b) changes in the discharge rate and firing pattern of the response to sound, and (c) changes in the effects of the neurotransmitters involved in the afferent and efferent pathways. 2. The first part of our report is based on the hypothesis that the encoding of sensory information needs a timer in order to be processed and stored, and that the hippocampal theta rhythm could contribute to the temporal organization. We have demonstrated that the guinea pig's auditory and visual neuronal discharge exhibits a temporal relationship (phase locking) to the hippocampal theta waves during wakefulness and sleep phases. 3. The concept that the neural network orga...

Cellular correlates of wakefulness and slow-wave sleep: evidence for a key role of inhibition

Current Opinion in Physiology

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Sleep-Dependent Potentiation in the Visual System Is at Odds with the Synaptic Homeostasis Hypothesis

Sleep, 2015

Two commentaries recently published in SLEEP came to very different conclusions regarding how data from a mouse model of sleep-dependent neural plasticity (orientation-specific response potentiation; OSRP) fit with the synaptic homeostasis hypothesis (SHY). To assess whether SHY offers an explanatory mechanism for OSRP, we present new data on how cortical neuron firing rates are modulated as a function of novel sensory experience and subsequent sleep in this model system. We carried out longitudinal extracellular recordings of single-neuron activity in the primary visual cortex across a period of novel visual experience and subsequent sleep or sleep deprivation. Spontaneous neuronal firing rates and visual responses were recorded from the same population of visual cortex neurons before control (blank screen) or novel (oriented grating) stimulus presentation, immediately after stimulus presentation, and after a period of subsequent ad lib sleep. Firing rate responses to visual stimul...

Fast Hemodynamic Responses in the Visual Cortex of the Awake Mouse

Journal of Neuroscience, 2013

Hemodynamic responses in mice and other species are typically measured under anesthesia. However, anesthesia could influence their relationship to neural activity. To investigate this relationship, we used optical imaging in mouse primary visual cortex (V1). Hemodynamic responses yielded clear maps of retinotopy in both anesthetized and awake mice. However, during wakefulness, responses were four times larger and twice as fast. These differences held whether we induced anesthesia with urethane or isoflurane and whether awake mice were stationary or running on a treadmill. With electrode recordings, we established that the effects of wakefulness reflect changes in neurovascular coupling, not in neural activity. By activating V1 directly via optogenetics, we replicated the effects of wakefulness in terms of timing but not of amplitude. We conclude that neurovascular coupling depends critically on anesthesia and wakefulness: during wakefulness, neural activity is followed by much stronger and quicker hemodynamic responses.

Characteristics of fMRI responses to visual stimulation in anesthetized vs. awake mice

2020

The functional characteristics of the mouse visual system have not previously been well explored using fMRI. In this research, we examined 9.4 T BOLD fMRI responses to visual stimuli of varying pulse durations (1 – 50 ms) and temporal frequencies (1 – 10 Hz) under ketamine and xylazine anesthesia, and compared fMRI responses of anesthetized and awake mice. Under anesthesia, significant positive BOLD responses were detected bilaterally in the major structures of the visual pathways, including the dorsal lateral geniculate nuclei, superior colliculus, lateral posterior nucleus of thalamus, primary visual area, and higher-order visual area. BOLD responses increased slightly with pulse duration, were maximal at 3 – 5 Hz stimulation, and significantly decreased at 10 Hz, which were all consistent with previous neurophysiological findings. When the mice were awake, the BOLD fMRI response was faster in all active regions and stronger in the subcortical areas compared with the anesthesia co...

Prolonged wakefulness alters neuronal responsiveness to local electrical stimulation of the neocortex in awake rats

Journal of Sleep Research, 2012

Prolonged wakefulness or a lack of sleep lead to cognitive deficits, but little is known about the underlying cellular mechanisms. We recently found that sleep deprivation affects spontaneous neuronal activity in the neocortex of sleeping and awake rats. While it is well known that synaptic responses are modulated by ongoing cortical activity, it remains unclear whether prolonged waking affects responsiveness of cortical neurons to incoming stimuli. By applying local electrical microstimulation to the frontal area of the neocortex, we found that after a 4-hour period of waking the initial neuronal response in the contralateral frontal cortex was stronger and more synchronous, and was followed by a more profound inhibition of neuronal spiking as compared to the control condition. These changes in evoked activity suggest increased neuronal excitability and indicate that after staying awake cortical neurons become transiently bistable. We propose that some of the detrimental effects of sleep deprivation may be a result of altered neuronal responsiveness to incoming intrinsic and extrinsic inputs.

Hour-long adaptation in the awake early visual system

Journal of Neurophysiology, 2015

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 >1 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 neu...

Two types of slow waves in anesthetized and sleeping brains

2018

Deep sleep and anesthesia have contrasting effects on memory, yet at the microscopic scale they appear to produce similar neural network dynamics consisting of slow waves associated with alternating transients of high activity (UP states) and silence (DOWN states). Here, UP and DOWN state dynamics are analyzed in cortical recordings from human, monkey, and rat and found to be robustly different between deep sleep and anesthesia. We found that the temporal statistics of UP and DOWN states is robustly different in natural slow-wave sleep compared to the slow-waves of anesthesia. Computational models predict that an interplay between noise and spike-frequency adaptation can yield a transition from sleep-like to anesthesia-like slow-wave dynamics. These predictions were confirmed by pharmacological manipulations in vitro, inducing a switch between the two types of slow-waves. The results show that the strong adaptation found in anesthesia, but not in sleep, can produce a different type ...

A Comparison of Visual Response Properties in the Lateral Geniculate Nucleus and Primary Visual Cortex of Awake and Anesthetized Mice

The Journal of neuroscience : the official journal of the Society for Neuroscience, 2016

The cerebral cortex of the mouse has become one of the most important systems for studying information processing and the neural correlates of behavior. Multiple studies have examined the first stages of visual cortical processing: primary visual cortex (V1) and its thalamic inputs from the dorsal lateral geniculate nucleus (dLGN), but more rarely in the lateral posterior nucleus (LP) in mice. Multiple single-unit surveys of dLGN and V1, both with electrophysiology and two-photon calcium imaging, have described receptive fields in anesthetized animals. Increasingly, awake animals are being used in physiological studies, so it is important to compare neuronal responses between awake and anesthetized state. We have performed a comprehensive survey of spatial and temporal response properties in V1, dLGN, and lateral posterior nucleus of both anesthetized and awake animals, using a common set of stimuli: drifting sine-wave gratings spanning a broad range of spatial and temporal paramete...

A transient cortical state with sleep-like sensory responses precedes emergence from general anesthesia in humans

eLife, 2018

During awake consciousness, the brain intrinsically maintains a dynamical state in which it can coordinate complex responses to sensory input. How the brain reaches this state spontaneously is not known. General anesthesia provides a unique opportunity to examine how the human brain recovers its functional capabilities after profound unconsciousness. We used intracranial electrocorticography and scalp EEG in humans to track neural dynamics during emergence from propofol general anesthesia. We identify a distinct transient brain state that occurs immediately prior to recovery of behavioral responsiveness. This state is characterized by large, spatially distributed, slow sensory-evoked potentials that resemble the K-complexes that are hallmarks of stage two sleep. However, the ongoing spontaneous dynamics in this transitional state differ from sleep. These results identify an asymmetry in the neurophysiology of induction and emergence, as the emerging brain can enter a state with a sl...