Sleep differentially affects early and late neuronal responses to sounds in auditory and perirhinal cortices

Abstract

Number of multimedia and 3D models: 0 Number of words for abstract (max 250): 171 Number of words for introduction (max 650): 596 Number of words for discussion (max 1500): 919Reduced behavioral responsiveness to sensory stimulation is at the core of sleep's definition, but it is still unclear how the sleeping brain responds differently to sensory stimuli. In the current study we recorded neuronal spiking responses to sounds along the cortical processing hierarchy of rats during wakefulness and natural sleep. Responses in auditory cortex only showed modest changes during sleep, whereas sleep robustly attenuated the responses of neurons in high-level perirhinal cortex. We also found that during NREM sleep, the response latency predicts the degree of sleep attenuation in individual neurons above and beyond their anatomical location. These results provide anatomical and temporal signatures of sensory disconnection during sleep and pave the way to understanding the underlying mechanisms.

Impaired top-down auditory processing despite extensive single-neuron responses during human sleep

“…Our results demonstrate the presence of robust neuronal and LFP HG power responses in the early auditory cortex with a similar magnitude of response in sleep and wakefulness. This is consistent with recent animal 3,4,22,24 and non-invasive human studies 5,6,25,29 . There was a stronger attenuation during sleep in regions beyond the auditory cortex and in late sustained responses (Fig.…”

“…There was a stronger attenuation during sleep in regions beyond the auditory cortex and in late sustained responses (Fig. 3g), as recently observed in the rat 4 . Notwithstanding the attenuation of responses downstream from A1 in some cases, most responses were not significantly decreased.…”

Dynamic Auditory Remapping Across the Sleep-Wake Cycle

“…These stimulus-dependent responses can potentially explain some of the discrepancies between sleep studies showing enhanced (Colrain and Campbell, 2007; Hall and Borbely, 1970; Nicholas et al, 2006; Yang and Wu, 2007), reduced (Czisch et al, 2002, 2004; Murata and Kameda, 1963) or preserved activity between sleep and wakefulness (Edeline et al, 2001; Issa and Wang, 2008; Nir et al, 2015; Peña et al, 1999). Furthermore, while responses across a neural population may show one pattern, a detailed investigation of single neurons has revealed heterogenous responses and different degrees of attenuation (Edeline et al, 2001; Issa and Wang, 2008; Nir et al, 2015; Peña et al, 1999; Sela et al, 2016, 2020). Specific properties at the neuronal level such as latency, selectivity or receptive field size (Edeline et al, 2001; Sela et al, 2020) may explain part of the patterns that are seen at the cortical level.…”

“…Furthermore, while responses across a neural population may show one pattern, a detailed investigation of single neurons has revealed heterogenous responses and different degrees of attenuation (Edeline et al, 2001; Issa and Wang, 2008; Nir et al, 2015; Peña et al, 1999; Sela et al, 2016, 2020). Specific properties at the neuronal level such as latency, selectivity or receptive field size (Edeline et al, 2001; Sela et al, 2020) may explain part of the patterns that are seen at the cortical level. The evidence gathered at the neuronal, population and cortical levels call for a comprehensive examination of a range of stimulus properties in order to unveil the interplay between conscious state and sensory mapping.…”

“…There is a wide consensus that some degree of sensory processing persists during sleep (Andrillon and Kouider, 2020; Arzi et al, 2012, 2014; Atienza et al, 2001; Canales-Johnson et al, 2020; Chennu and Bekinschtein, 2012; Hennevin et al, 2007; Velluti, 1997). Neuroimaging and electrophysiology studies in humans (Atienza et al, 2001; Bastuji and García-Larrea, 1999; Colrain and Campbell, 2007; Czisch et al, 2002, 2009; Portas et al, 2000; Schabus et al, 2012; Wilf et al, 2016) and animals (Edeline et al, 2001; Issa and Wang, 2008; Nir et al, 2015; Sela et al, 2020) demonstrate clear brain activity in response to sensory stimuli in sleep. However, it remains unclear precisely how sensory-related neural activity changes during sleep.…”