Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Abstract

Most sensory stimuli do not reach conscious perception during sleep. It has been thought that the thalamus prevents the relay of sensory information to cortex during sleep, but the consequences for cortical responses to sensory signals in this physiological state remain unclear. We recorded from two auditory cortical areas downstream of the thalamus in naturally sleeping marmoset monkeys. Single neurons in primary auditory cortex (A1) either increased or decreased their responses during sleep compared to wakefulness. In lateral belt (LB), a secondary auditory cortical area, the response modulation was also bidirectional and showed no clear systematic depressive effect of sleep. When averaged across neurons, sound-evoked activity in these two auditory cortical areas was surprisingly well-preserved during sleep. Neural responses to acoustic stimulation were present during both slow-wave (SWS) and rapid-eye movement (REM) sleep, were repeatedly observed over multiple sleep cycles, and demonstrated similar discharge patterns to the responses recorded during wakefulness in the same neuron. Our results suggest that the thalamus is not as effective a gate for the flow of sensory information as previously thought. At the cortical stage, a novel pattern of activation/deactivation appears across neurons. Since the neural signal reaches as far as secondary auditory cortex, this leaves open the possibility of altered sensory processing of auditory information during sleep.

Altered Neural Responses to Sounds in Primate Primary Auditory Cortex during Slow-Wave Sleep

“…Neural data were collected from primary auditory cortex (A1) in four hemispheres of three common marmosets (Callithrix jacchus) (one male, two female) that were also used in our previous study (Issa and Wang, 2008). Animals were adapted to sit in a primate restraint chair for two weeks before a surgery implanting two stainless steel head posts for fixation of the head.…”

“…The EEG and video monitoring (sensitive in the infrared range) of the face and tail were used to assess an animal's behavioral state. Behavioral state was readily identified using standard human sleep scoring techniques (Carskadon and Rechtschaffen, 2000), and details are provided in a previous study (Issa and Wang, 2008). Here, it is important to note that sounds did not awaken the animals even when played at the loudest intensities used in this study.…”

“…Neurons were held for an average of 90 min to allow comparison of neural responses across different states [marmoset sleep cycle Ϸ 50 min (Crofts et al, 2001)]. Details of the identification of A1 are given previously (Issa and Wang, 2008).…”

“…The loss of conscious awareness in sleep is often compared with the state induced by anesthesia, but this may only be a superficial comparison as evoked potential (Nielsen-Bohlman et al, 1991;Bastuji et al, 2002) and imaging (Portas et al, 2000) studies in humans and, more recently, single neuron recordings in nonhuman primates (Issa and Wang, 2008) have shown a surprising degree of activation in response to sounds in auditory cortex during sleep in a manner that qualitatively resembles that during wakefulness rather than anesthesia. The finding that acoustic information is still reaching auditory cortex during sleep is also inconsistent with the prevailing view that a thalamic gate insulates the cortex from the external sensory environment (Steriade, 2003), as had been suggested by neural recordings across auditory (Edeline et al, 2000), visual (Livingstone and Hubel, 1981), and somatosensory (Mariotti et al, 1989) thalamus during sleep.…”

Disruption of hierarchical predictive coding during sleep

“…Alternatively, it has been proposed that sleep may induce a loss of integration at a late stage of cortical processing (3)(4)(5). Indeed, preserved activation of primary sensory cortices has been reported in electrophysiological studies in animals (6)(7)(8)(9) and in neuroimaging studies in humans (10)(11)(12). Furthermore, stimuli that have behavioral relevance, such as hearing one's name, may induce a broad spread of activation into higher cortical areas (10) and evoke late scalp event-related potentials (ERPs) (13).…”