Cell and circuit origins of fast network oscillations in the mammalian main olfactory bulb

Neural synchrony generates fast network oscillations throughout the brain, including the main olfactory bulb (MOB), the first processing station of the olfactory system. Identifying the mechanisms synchronizing neurons in the MOB will be key to understanding how network oscillations support the coding of a high-dimensional sensory space. Here, using paired recordings and optogenetic activation of glomerular sensory inputs in MOB slices, we uncovered profound differences in principal mitral cell (MC) vs. tufted cell (TC) spike-time synchrony: TCs robustly synchronized across fast- and slow-gamma frequencies, while MC synchrony was weaker and concentrated in slow-gamma frequencies. Synchrony among both cell types was enhanced by shared glomerular input but was independent of intraglomerular lateral excitation. Cell-type differences in synchrony could also not be traced to any difference in the synchronization of synaptic inhibition. Instead, greater TC than MC synchrony paralleled the more periodic firing among resonant TCs than MCs and emerged in patterns consistent with densely synchronous network oscillations. Collectively, our results thus reveal a mechanism for parallel processing of sensory information in the MOB via differential TC vs. MC synchrony, and further contrast mechanisms driving fast network oscillations in the MOB from those driving the sparse synchronization of irregularly-firing principal cells throughout cortex.

Cell and circuit origins of fast network oscillations in the mammalian main olfactory bulb

Neural synchrony generates fast network oscillations throughout the brain, including the main olfactory bulb (MOB), the first processing station of the olfactory system. Identifying the mechanisms synchronizing neurons in the MOB will be key to understanding how network oscillations support the coding of a high-dimensional sensory space. Here, using paired recordings and optogenetic activation of glomerular sensory inputs in MOB slices, we uncovered profound differences in principal mitral cell (MC) vs. tufted cell (TC) spike-time synchrony: TCs robustly synchronized across fast- and slow-gamma frequencies, while MC synchrony was weaker and concentrated in slow-gamma frequencies. Synchrony among both cell types was enhanced by shared glomerular input but was independent of intraglomerular lateral excitation. Cell-type differences in synchrony could also not be traced to any difference in the synchronization of synaptic inhibition. Instead, greater TC than MC synchrony paralleled the more periodic firing among resonant TCs than MCs and emerged in patterns consistent with densely synchronous network oscillations. Collectively, our results thus reveal a mechanism for parallel processing of sensory information in the MOB via differential TC vs. MC synchrony, and further contrast mechanisms driving fast network oscillations in the MOB from those driving the sparse synchronization of irregularly-firing principal cells throughout cortex.

Alpha-to-beta- and gamma-band activity reflect predictive coding in affective visual processing

Processing of negative affective pictures typically leads to desynchronization of alpha-to-beta frequencies (ERD) and synchronization of gamma frequencies (ERS). Given that in predictive coding higher frequencies have been associated with prediction errors, while lower frequencies have been linked to expectations, we tested the hypothesis that alpha-to-beta ERD and gamma ERS induced by aversive pictures are associated with expectations and prediction errors, respectively. We recorded EEG while volunteers were involved in a probabilistically cued affective picture task using three different negative valences to produce expectations and prediction errors. Our data show that alpha-to-beta band activity was related to the expected valence of the stimulus as predicted by a cue. The absolute mismatch of the expected and actual valence, which denotes an absolute prediction error was related to gamma band activity. This demonstrates that top-down predictions and bottom-up prediction errors are represented in specific spectral patterns associated with affective picture processing.

Neocortical rhythm entrainment by parvalbumin-positive interneurons across cortical layers

Neocortical interneurons provide local inhibition responsible for organizing neuronal activity into brain oscillations that subserve several functions such as memory, attention and neuronal communication. However, little is known about the contribution of interneurons to the entrainment of neocortical oscillations across cortical layers. Here, using layer-specific optogenetic stimulations with micro-Light-Emitting-Diode (μLED) arrays, directed toward parvalbumin-expressing (PV) interneurons in non-anesthetized awake mice, we find that supragranular layer stimulations of PV neurons were most efficient at entraining supragranular layer neurons and local field potential (LFP) oscillations at gamma frequencies (γ: 25 - 80 Hz), whereas infragranular layer stimulation of PV neurons better entrained delta (δ: 2 - 5 Hz) and theta (θ: 6 - 10 Hz) frequency LFP oscillations. We found that PV neurons tightly control the transmission of multiple rhythms to the network across cortical layers in an orientation-selective manner. Intrinsic resonant properties of neurons could underlie such layer-specific properties of rhythm entrainment.

Investigating the effects of transcranial alternating current stimulation on primary somatosensory cortex

Near-threshold tactile stimuli perception and somatosensory temporal discrimination threshold (STDT) are encoded in the primary somatosensory cortex (S1) and largely depend on alpha and beta S1 rhythm. Transcranial alternating current stimulation (tACS) is a non-invasive neurophysiological technique that allows cortical rhythm modulation. We investigated the effects of tACS delivered over S1 at alpha, beta, and gamma frequencies on near-threshold tactile stimuli perception and STDT, as well as phase-dependent tACS effects on near-threshold tactile stimuli perception in healthy subjects. In separate sessions, we tested the effects of different tACS montages, and tACS at the individualised S1 μ-alpha frequency peak, on STDT and near-threshold tactile stimuli perception. We found that tACS applied over S1 at alpha, beta, and gamma frequencies did not modify STDT or near-threshold tactile stimuli perception. Moreover, we did not detect effects of tACS phase or montage. Finally, tACS did not modify near-threshold tactile stimuli perception and STDT even when delivered at the individualised μ-alpha frequency peak. Our study showed that tACS does not alter near-threshold tactile stimuli or STDT, possibly due to the inability of tACS to activate deep S1 layers. Future investigations may clarify tACS effects over S1 in patients with focal dystonia, whose pathophysiology implicates increased STDT.

Intermuscular coherence between homologous muscles during dynamic and static movement periods of bipedal squatting

It is largely unexplored how the central nervous system achieves coordination of homologous muscles of the upper and lower body within a compound whole body movement, and to what extent this neural drive is modulated between different movement periods and muscles. Using intermuscular coherence analysis, we show that homologous muscle functions are mediated through common oscillatory input that extends over alpha, beta, and gamma frequencies with different synchronization patterns at different movement periods.

Interhemispheric transfer of working memories

SummaryVisual working memory (WM) storage is largely independent between the left and right visual hemifields/cerebral hemispheres, yet somehow WM feels seamless. We studied how WM is integrated across hemifields by recording neural activity bilaterally from lateral prefrontal cortex. An instructed saccade during the WM delay shifted the remembered location from one hemifield to the other. Before the shift, spike rates and oscillatory power showed clear signatures of memory laterality. After the shift, the lateralization inverted, consistent with transfer of the memory trace from one hemisphere to the other. Transferred traces initially used different neural ensembles from feedforward-induced ones but they converged at the end of the delay. Around the time of transfer, synchrony between the two prefrontal hemispheres peaked in theta and low-gamma frequencies, with a directionality consistent with memory trace transfer. This illustrates how dynamics between the two cortical hemispheres can stitch together WM traces across visual hemifields.

Neuronal pathway and signal modulation for motor communication

The knowledge of the mechanisms of motor imagery (MI) is very important for the development of braincomputer interfaces. Depending on neurophysiological cortical activity, MI can be divided into two categories: visual imagery (VI) and kinesthetic imagery (KI). Our magnetoencephalography (MEG) experiments with ten untrained subjects provided evidences that inhibitory control plays a dominant role in KI. We found that communication between inferior parietal cortex and frontal cortex is realised in the mu-frequency range. We also pinpointed three gamma frequencies to be used for motor command communication. The use of artificial intelligence allowed us to classify MI of left and right hands with maximal classification accuracy using the brain activity encoded in the identified gamma frequencies which were then proposed to be used for communication of specifics. Mu-activity was identified as the carrier of gamma-activity between these areas by means of phase-amplitude coupling similar to the modern day radio wave transmission.

Central thalamus modulates consciousness by controlling layer-specific cortical interactions

Consciousness is the capacity to experience one’s environment and internal states. The minimal mechanisms sufficient to produce this experience, the neural correlates of consciousness (NCC), are thought to involve thalamocortical and intracortical interactions, but the key operations and circuit paths are unclear. We simultaneously recorded neural activity in central thalamus and across layers of fronto-parietal cortex in awake, sleeping and anesthetized macaques. Spiking activity was selectively reduced in deep cortical layers and thalamus during unconsciousness, as were intracolumnar and interareal interactions at alpha and gamma frequencies. Gamma-frequency stimulation, when focused on the central lateral thalamus of anesthetized macaques, counteracted these neural changes and restored consciousness. These findings suggest that the NCC involve both corticocortical feedforward and feedback pathways coordinated with intracolumnar and thalamocortical loops.SummaryStimulation of central lateral thalamus counters anesthesia to restore wake cortical dynamics and consciousness.