Set and setting: How behavioral state regulates sensory function and plasticity

Abstract

Recently developed neuroimaging and electrophysiological techniques are allowing us to answer fundamental questions about how behavioral states regulate our perception of the external environment. Studies using these techniques have yielded surprising insights into how sensory processing is affected at the earliest stages by attention and motivation, and how new sensory information received during wakefulness (e.g., during learning) continues to affect sensory brain circuits (leading to plastic changes) during subsequent sleep. This review aims to describe how brain states affect sensory response properties among neurons in primary and secondary sensory cortices, and how this relates to psychophysical detection thresholds and performance on sensory discrimination tasks. This is not intended to serve as a comprehensive overview of all brain states, or all sensory systems, but instead as an illustrative description of how three specific state variables (attention, motivation, and vigilance [i.e., sleep vs. wakefulness]) affect sensory systems in which they have been best studied.

Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity

“…However, stimulus presentation alone does not affect primary visual cortex (V1) neurons, which show response changes only after a period of subsequent sleep. During poststimulus nonrapid eye movement (NREM) sleep, LGN neuron overall spike-field coherence (SFC) with V1 delta (0.5-4 Hz) and spindle (7)(8)(9)(10)(11)(12)(13)(14)(15) Hz) oscillations increased, with neurons most responsive to the presented stimulus showing greater SFC. To test whether coherent communication between LGN and V1 was essential for cortical plasticity, we first tested the role of layer 6 corticothalamic (CT) V1 neurons in coherent firing within the LGN-V1 network.…”

“…The sleep-dependent mechanisms driving these changes have remained elusive. Sleep-associated changes in network activity (1,6,7,9,10), neuromodulator tone (11), transcription (4), translation (4), and protein phosphorylation (2,3) have all been correlated with cortical plasticity following novel experiences (12). In recent years, neuroscientists have speculated that the high-amplitude, low-frequency thalamocortical oscillations that characterize nonrapid eye movement (NREM) sleep play a critical role in promoting sensory cortical plasticity and learning (12).…”

“…Sleep-associated changes in network activity (1,6,7,9,10), neuromodulator tone (11), transcription (4), translation (4), and protein phosphorylation (2,3) have all been correlated with cortical plasticity following novel experiences (12). In recent years, neuroscientists have speculated that the high-amplitude, low-frequency thalamocortical oscillations that characterize nonrapid eye movement (NREM) sleep play a critical role in promoting sensory cortical plasticity and learning (12). While it has been hypothesized that such NREM oscillations promote general synaptic "downscaling" (13), converging data suggest that they could instead promote synaptic strengthening (5)(6)(7)9).…”

Effects of Blast Exposure on Subjective and Objective Sleep Measures in Combat Veterans with and without PTSD

“…Collection of objective assessments given more proximally to blast exposure is necessary to ascertain the exactitude of self-reports of previous blast or TBI. Given the role of sleep in neuroplasticity, [61][62][63] changes in objective sleep parameters may be detectable in the immediate aftermath of blast exposure, which may normalize over time and/or with the remission of concussive symptoms. Sleep assessments more proximal to the time of injury are necessary to provide insights into the impact of sleep preservation, or of sleep disturbance, on the trajectory of TBI recovery and of PTSD.…”

Sensory response in host and engrafted astrocytes of adult brain in Vivo

“…Sensation, a basic neural function, determines the brain's state and is essential for motivation, emotion, attention, consciousness, and arousal (Aton, ). Some of the important roles of astrocytes are to respond to sensory stimulation and to participate in sensory processing (Wang et al, ).…”