Primate somatosensory cortical neurons are entrained to both spontaneous and peripherally evoked spindle oscillations.

Recurrent thalamocortical circuits produce a number of rhythms critical to brain function. In slow-wave sleep, spindles (7-16 Hz) are a prominent spontaneous oscillation generated by thalamic circuits and triggered by cortical slow waves. In wakefulness and under anesthesia, brief peripheral sensory stimuli can evoke 10-Hz reverberations due potentially to similar thalamic mechanisms. Functionally, sleep spindles and peripherally evoked spindles may play a role in memory consolidation and perception, respectively. Yet, rarely have the circuits involved in these two rhythms been compared in the same animals and never in primates. Here, we investigated the entrainment of primary somatosensory cortex (S1) neurons to both rhythms in ketamine-sedated macaques. First, we compared spontaneous spindles in sedation and natural sleep to validate the model. Then, we quantified entrainment with spike-field coherence and phase-locking statistics. We found that S1 neurons entrained to spontaneous sleep spindles were also entrained to the evoked spindles, although entrainment strength and phase systematically differed. Our results indicate that the spindle oscillations triggered by top-down spontaneous cortical activity and bottom-up peripheral input share a common cortical substrate.NEW & NOTEWORTHY Brief sensory stimuli evoke 10-Hz oscillations in thalamocortical neuronal activity and in perceptual thresholds. The mechanisms underlying this evoked rhythm are not well understood but are thought to be similar to those generating sleep spindles. We directly compared the entrainment of cortical neurons to both spontaneous spindles and peripherally evoked oscillations in sedated monkeys. We found that the entrainment strengths to each rhythm were positively correlated, although with differing entrainment phases, implying involvement of similar networks.

A chronic neural interface to the macaque dorsal column nuclei.

The dorsal column nuclei (DCN) of the brain stem contain secondary afferent neurons, which process ascending somatosensory information. Most of the known physiology of the DCN in primates has been acquired in acute experiments with anesthetized animals. Here, we developed a technique to implant a multielectrode array (MEA) chronically in the DCN of macaque monkeys to enable experiments with the animals awake. Two monkeys were implanted with brain-stem MEAs for 2-5 mo with no major adverse effects. Responses of the cuneate and gracile nuclei were quantified at the level of both field potentials and single units. Tactile receptive fields (RFs) were identified for 315 single units. A subset of these units had very regular spiking patterns with spike frequencies predominantly in the alpha band (8-14 Hz). The stability of the neuronal recordings was assessed with a novel analysis that identified units by their mean spike waveform and by the spike-triggered average of activity on all other electrodes in the array. Fifty-six identified neurons were observed over two or more sessions and in a few cases for as long as 1 mo. RFs of stable neurons were largely consistent across days. The results demonstrate that a chronic DCN implant in a macaque can be safe and effective, yielding high-quality unit recording for several months. The unprecedented access to these nuclei in awake primates should lead to a better understanding of their role in sensorimotor behavior.

Somatosensory encoding with cuneate nucleus microstimulation: Detection of artificial stimuli.

The sense of touch and proprioception are critical to movement control. After spinal cord injury, these senses may be restored with direct, electrical microstimulation of the brain as part of a complete sensorimotor neuroprosthesis. The present study was designed to test, in part, the hypothesis that the cuneate nucleus (CN) of the brainstem is a suitable site to encode somatosensory information. Two rhesus macaques were implanted with microelectrode arrays providing chronic access to the CN. The monkeys were trained on an active touch oddity task to detect vibrotactile stimuli. When the vibrotactile stimuli were replaced with electrical stimuli delivered to the CN, initial detection probabilities were near chance. Detection performance improved over time, reaching a plateau after about 10 daily sessions. At plateau performance, the monkeys exhibited detection probabilities that were 68-80% higher than the chance probability. Finally, detection probability was quantified as a function of stimulus amplitude. The resulting psychometric curve showed a detection threshold of 45 µA for 100-Hz stimulus trains. These behavioral data are the first to show that artificial CN activation is sufficient for perception. The results are consistent with our hypothesis and motivate future tests of the CN as a somatosensory encoding site.