Showing papers in "Journal of Neurophysiology in 2020"

Tactile innervation densities across the whole body.

Abstract: The skin is our largest sensory organ and innervated by afferent fibers carrying tactile information to the spinal cord and onto the brain. The density with which different classes of tactile affer...

Situating the Left-Lateralized Language Network in the Broader Organization of Multiple Specialized Large-Scale Distributed Networks

Abstract: This research shows that a language network can be identified within individuals using functional connectivity. Organizational details reveal that the language network shares a common spatial motif...

Parallel distributed networks dissociate episodic and social functions within the individual.

Abstract: Two distributed, interdigitated networks exist within the bounds of the canonical default network. Here we used repeated scanning of individuals, across three independent samples, to provide eviden...

Challenges to the central nervous system during human spaceflight missions to Mars

Abstract: Space travel presents a number of environmental challenges to the central nervous system, including changes in gravitational acceleration that alter the terrestrial synergies between perception and...

Estimation of self-sustained activity produced by persistent inward currents using firing rate profiles of multiple motor units in humans.

Abstract: Persistent inward calcium and sodium currents (IP) activated during motoneuron recruitment help synaptic inputs maintain self-sustained firing until derecruitment. Here, we estimate the contribution of the IP to self-sustained firing in human motoneurons of varying recruitment threshold by measuring the difference in synaptic input needed to maintain minimal firing once the IP is fully activated compared with the larger synaptic input required to initiate firing before full IP activation. Synaptic input to ≈20 dorsiflexor motoneurons simultaneously recorded during ramp contractions was estimated from firing profiles of motor units decomposed from high-density surface electromyography (EMG). To avoid errors introduced when using high-threshold units firing in their nonlinear range, we developed methods where the lowest threshold units firing linearly with force were used to construct a composite (control) unit firing rate profile to estimate synaptic input to higher threshold (test) units. The difference in the composite firing rate (synaptic input) at the time of test unit recruitment and derecruitment (ΔF = Frecruit - Fderecruit) was used to measure IP amplitude that sustained firing. Test units with recruitment thresholds 1-30% of maximum had similar ΔF values, which likely included both slow and fast motor units activated by small and large motoneurons, respectively. This suggests that the portion of the IP that sustains firing is similar across a wide range of motoneuron sizes.NEW & NOTEWORTHY A new method of estimating synaptic drive to multiple, simultaneously recorded motor units provides evidence that the portion of the depolarizing drive from persistent inward currents that contributes to self-sustained firing is similar across motoneurons of different sizes.

Next-generation neural mass and field modeling.

Abstract: The Wilson-Cowan population model of neural activity has greatly influenced our understanding of the mechanisms for the generation of brain rhythms and the emergence of structured brain activity. As well as the many insights that have been obtained from its mathematical analysis, it is now widely used in the computational neuroscience community for building large-scale in silico brain networks that can incorporate the increasing amount of knowledge from the Human Connectome Project. Here, we consider a neural population model in the spirit of that originally developed by Wilson and Cowan, albeit with the added advantage that it can account for the phenomena of event-related synchronization and desynchronization. This derived mean-field model provides a dynamic description for the evolution of synchrony, as measured by the Kuramoto order parameter, in a large population of quadratic integrate-and-fire model neurons. As in the original Wilson-Cowan framework, the population firing rate is at the heart of our new model; however, in a significant departure from the sigmoidal firing rate function approach, the population firing rate is now obtained as a real-valued function of the complex-valued population synchrony measure. To highlight the usefulness of this next-generation Wilson-Cowan style model, we deploy it in a number of neurobiological contexts, providing understanding of the changes in power spectra observed in electro- and magnetoencephalography neuroimaging studies of motor cortex during movement, insights into patterns of functional connectivity observed during rest and their disruption by transcranial magnetic stimulation, and to describe wave propagation across cortex.

A literature review on the neurophysiological underpinnings and cognitive effects of transcutaneous vagus nerve stimulation: challenges and future directions.

Abstract: Brain stimulation approaches are important to gain causal mechanistic insights into the relevance of functional brain regions and/or neurophysiological systems for human cognitive functions. In recent years, transcutaneous vagus nerve stimulation (tVNS) has attracted considerable popularity. It is a noninvasive brain stimulation technique based on the stimulation of the vagus nerve. The stimulation of this nerve activates subcortical nuclei, such as the locus coeruleus and the nucleus of the solitary tract, and from there, the activation propagates to the cortex. Since tVNS is a novel stimulation technique, this literature review outlines a brief historical background of tVNS, before detailing underlying neurophysiological mechanisms of action, stimulation parameters, cognitive effects of tVNS on healthy humans, and, lastly, current challenges and future directions of tVNS research in cognitive functions. Although more research is needed, we conclude that tVNS, by increasing norepineprine (NE) and gamma-aminobutyric acid (GABA) levels, affects NE- and GABA-related cognitive performance. The review provides detailed background information how to use tVNS as a neuromodulatory tool in cognitive neuroscience and outlines important future leads of research on tVNS.

The "embreathment" illusion highlights the role of breathing in corporeal awareness.

Abstract: Our body is the only object we sense from the inside; however, it is unclear how much inner physiology contributes to the global sensation of having a body and controlling it. We combine respiratio...

Reaching decisions during ongoing movements.

Abstract: Neurophysiological studies suggest that when decisions are made between concrete actions, the selection process involves a competition between potential action representations in the same sensorimotor structures involved in executing those actions. However, it is unclear how such models can explain situations, often encountered during natural behavior, in which we make decisions while were are already engaged in performing an action. Does the process of deliberation characterized in classical studies of decision-making proceed the same way when subjects are deciding while already acting? In the present study, human subjects continuously tracked a target moving in the horizontal plane and were occasionally presented with a new target to which they could freely choose to switch at any time, whereupon it became the new tracked target. We found that the probability of choosing to switch increased with decreasing distance to the new target and increasing size of the new target relative to the tracked target, as well as when the direction to the new target was aligned (either toward or opposite) to the current tracking direction. However, contrary to our expectations, subjects did not choose targets that minimized the energetic costs of execution, as calculated by a biomechanical model of the arm. When the constraints of continuous tracking were removed in variants of the task involving point-to-point movements, the expected preference for lower cost choices was seen. These results are discussed in the context of current theories of nested feedback control, internal models of forward dynamics, and high-dimensional neural spaces.NEW & NOTEWORTHY Current theories of decision-making primarily address how subjects make decisions before executing selected actions. However, in our daily lives we often make decisions while already performing some action (e.g., while playing a sport or navigating through a crowd). To gain insight into how current theories can be extended to such "decide-while-acting" scenarios, we examined human decisions during continuous manual tracking and found some intriguing departures from how decisions are made in classical "decide-then-act" paradigms.

Assessing explicit strategies in force field adaptation.

Abstract: While the contribution of explicit learning has been increasingly studied in visuomotor adaptation, its contribution to force field adaptation has not been studied extensively. We employed two nove...

Separation of hemodynamic signals from GCaMP fluorescence measured with wide-field imaging.

Abstract: This paper addresses a well-known and strong source of contamination in wide-field calcium-imaging data: hemodynamics. To guide researchers toward the best method to separate calcium signals from h...

Continuous reports of sensed hand position during sensorimotor adaptation.

Abstract: Sensorimotor adaptation operates in an obligatory manner. Qualitatively, subjective reports obtained after adaptation demonstrate that, in many conditions, participants are unaware of significant c...

Neural and muscular determinants of maximal rate of force development.

Abstract: An important limitation of human performance is the ability to generate explosive movements by means of rapid development of muscle force. The physiological determinants of this ability, however, a...

Savings in sensorimotor adaptation without an explicit strategy

Abstract: The hallmark of long-term retention of sensorimotor adaptation is a faster relearning when similar perturbations are encountered again. However, what processes underlie this saving effect is in debate. Though motor adaptation is traditionally viewed as a type of procedural learning, its savings has been recently shown to be solely based on a quick recall of explicit adaptation strategy. Here, we showed that adaptation to a novel error-invariant perturbation without an explicit strategy could enable subsequent savings. We further showed that adaptation to gradual perturbations could enable savings, which was supported by enhanced implicit learning. Our study provides supporting evidence that long-term retention of motor adaptation is possible without forming or recalling a cognitive strategy, and the interplay between implicit and explicit learning critically depends on the specifics of learning protocol and available sensory feedback.NEW & NOTEWORTHY Savings in motor learning sometimes refers to faster learning when one encounters the same perturbation again. Previous studies assert that forming a cognitive strategy for countering perturbations is necessary for savings. We used novel experimental techniques to prevent the formation of a cognitive strategy during initial adaptation and found that savings still existed during relearning. Our findings suggest that savings in sensorimotor adaptation do not exclusively depend on forming and recalling an explicit strategy.

Electrophysiological markers of cochlear function correlate with hearing-in-noise performance among audiometrically normal subjects

Abstract: Hearing loss caused by noise exposure, ototoxic drugs, or aging results from the loss of sensory cells, as reflected in audiometric threshold elevation. Animal studies show that loss of hair cells can be preceded by loss of auditory-nerve peripheral synapses, which likely degrades auditory processing. While this condition, known as cochlear synaptopathy, can be diagnosed in mice by a reduction of suprathreshold cochlear neural responses, its diagnosis in humans remains challenging. To look for evidence of cochlear nerve damage in normal hearing subjects, we measured their word recognition performance in difficult listening environments and compared it to cochlear function as assessed by otoacoustic emissions and click-evoked electrocochleography. Several electrocochleographic markers were correlated with word scores, whereas distortion product otoacoustic emissions were not. Specifically, the summating potential (SP) was larger and the cochlear nerve action potential (AP) was smaller in those with the worst word scores. Adding a forward masker or increasing stimulus rate reduced SP in the worst performers, suggesting that this potential includes postsynaptic components as well as hair cell receptor potentials. Results suggests that some of the variance in word scores among listeners with normal audiometric threshold arises from cochlear neural damage.NEW & NOTEWORTHY Recent animal studies suggest that millions of people may be at risk of permanent impairment from cochlear synaptopathy, the age-related and noise-induced degeneration of neural connections in the inner ear that "hides" behind a normal audiogram. This study examines electrophysiological responses to clicks in a large cohort of subjects with normal hearing sensitivity. The resultant correlations with word recognition performance are consistent with an important contribution cochlear neural damage to deficits in hearing in noise abilities.

A review of efferent cholinergic synaptic transmission in the vestibular periphery and its functional implications

Abstract: It has been over 60 years since peripheral efferent vestibular terminals were first identified in mammals, and yet the function of the efferent vestibular system remains obscure. One reason for the...

Environmental consistency modulation of error sensitivity during motor adaptation is explicitly controlled.

Abstract: The consistency of an external perturbation modulates error sensitivity and the motor response. The roles of explicit and implicit processes in this modulation are unknown. We show that when humans...

Neural shutdown under stress: an evolutionary perspective on spreading depolarization

Abstract: Neural function depends on maintaining cellular membrane potentials as the basis for electrical signaling. Yet, in mammals and insects, neuronal and glial membrane potentials can reversibly depolar...

A mean-field approach to the dynamics of networks of complex neurons, from nonlinear Integrate-and-Fire to Hodgkin-Huxley models

Abstract: We present a mean-field formalism able to predict the collective dynamics of large networks of conductance-based interacting spiking neurons. We apply this formalism to several neuronal models, from the simplest Adaptive Exponential Integrate-and-Fire model to the more complex Hodgkin-Huxley and Morris-Lecar models. We show that the resulting mean-field models are capable of predicting the correct spontaneous activity of both excitatory and inhibitory neurons in asynchronous irregular regimes, typical of cortical dynamics. Moreover, it is possible to quantitatively predict the population response to external stimuli in the form of external spike trains. This mean-field formalism therefore provides a paradigm to bridge the scale between population dynamics and the microscopic complexity of the individual cells physiology.NEW & NOTEWORTHY Population models are a powerful mathematical tool to study the dynamics of neuronal networks and to simulate the brain at macroscopic scales. We present a mean-field model capable of quantitatively predicting the temporal dynamics of a network of complex spiking neuronal models, from Integrate-and-Fire to Hodgkin-Huxley, thus linking population models to neurons electrophysiology. This opens a perspective on generating biologically realistic mean-field models from electrophysiological recordings.

The gravitational imprint on sensorimotor planning and control.

Abstract: Humans excel at learning complex tasks, and elite performers such as musicians or athletes develop motor skills that defy biomechanical constraints. All actions require the movement of massive bodi...

Early gamma-oscillations as correlate of localized nociceptive processing in primary sensorimotor cortex.

Abstract: Recent studies put forward the idea that stimulus-evoked gamma-band oscillations (GBOs; 30-100 Hz) play a specific role in nociception. So far, evidence for the specificity of GBOs for nociception, their possible involvement in nociceptive sensory discriminatory abilities, and knowledge regarding their cortical sources is just starting to grow. To address these questions, we used electroencephalography (EEG) to record brain activity evoked by phasic nociceptive laser stimuli and tactile stimuli applied at different intensities to the right hand and foot of 12 healthy volunteers. The EEG was analyzed in the time domain to extract phase-locked event-related brain potentials (ERPs) and in three regions of interest in the time-frequency domain (delta/theta, 40-Hz gamma, 70-Hz gamma) to extract stimulus-evoked changes in the magnitude of non-phase-locked brain oscillations. Both nociceptive and tactile stimuli, matched with respect to subjective intensity, elicited phase locked ERPs of increasing amplitude with increasing stimulus intensity. In contrast, only nociceptive stimuli elicited a significant enhancement of GBOs (65-85 Hz, 150-230 ms after stimulus onset), whose magnitude encoded stimulus intensity, whereas tactile stimuli led to a GBO decrease. Following nociceptive hand stimulation, the topographical distribution of GBOs was maximal at contralateral electrode C3, whereas maximum activity following foot stimulation was recorded at the midline electrode Cz, compatible with generation of GBOs in the representations of the hand and foot of the primary sensorimotor cortex, respectively. The differential behavior of high-frequency GBOs and low-frequency 40-Hz GBOs is indicating different functional roles and regions in sensory processing.NEW & NOTEWORTHY Gamma-band oscillations show hand-foot somatotopy compatible with generation in primary sensorimotor cortex and are present following nociceptive but not tactile stimulation of the hand and foot in humans.

Somatosensory changes associated with motor skill learning.

Abstract: Somatosensory processing has been implicated in motor adaptation, where performance recovers from a perturbation such as a force field. We investigated somatosensory function during motor skill lea...

Inability to increase the neural drive to muscle is associated with task failure during submaximal contractions

Abstract: We investigated changes in motor unit (MU) behavior and vasti-muscle contractile properties during sustained submaximal fatiguing contractions with a new time-domain tracking technique to understand the mechanisms responsible for task failure. Sixteen participants performed a nonfatiguing 15-s isometric knee extension at 50% of the maximum voluntary (MVC) torque, followed by a 30% MVC sustained contraction until exhaustion. Two grids of 64 surface electromyography electrodes were placed over vastus medialis and lateralis. Signals were decomposed into MU discharge times and the MUs from the 30% MVC sustained contraction were followed until task failure by overlapping decomposition intervals. These MUs were then tracked between 50% and 30% MVC. During the sustained fatiguing contraction, MUs of the two muscles decreased their discharge rate until ∼40% of the endurance time, referred to as the reversal time, and then increased their discharge rate until task failure. This reversal in firing behavior predicted total endurance time and was matched by opposite changes in twitch force (increase followed by a decrease). Despite the later increase in MU firing rates, peak discharge rates at task failure did not reach the frequency attained during a nonfatiguing 50% MVC contraction. These results show that changes in MU firing properties are influenced by adjustments in contractile properties during the course of the contraction, allowing the identification of two phases. Nevertheless, the contraction cannot be sustained, possibly because of progressive motoneuron inhibition/decreased excitability, as the later increase in firing rate saturates at a much lower frequency compared with a higher-force nonfatiguing contraction.NEW & NOTEWORTHY Motor unit firing and contractile properties during a submaximal contraction until failure were assessed with a new tracking technique. Two distinct phases in firing behavior were observed, which compensated for changes in twitch area and predicted time to failure. However, the late increase in firing rate was below the rates attained in absence of fatigue, which points to an inability of the central nervous system to sufficiently increase the neural drive to muscle with fatigue.

Differences in estimated persistent inward currents between ankle flexors and extensors in humans

Abstract: Persistent inward currents (PICs) are responsible for amplifying motoneuronal synaptic inputs and contribute to generating normal motoneuron activation. Delta-F (ΔF) is a well-established method that estimates PICs in humans indirectly from firing patterns of individual motor units. Traditionally, motor unit firing patterns are obtained by manually decomposing electromyography (EMG) signals recorded through intramuscular electrodes (iEMG). A previous iEMG study has shown that in humans the elbow extensors have higher ΔF than the elbow flexors. In this study, EMG signals were collected from the ankle extensors and flexors using high-density surface array electrodes during isometric sitting and standing at 10-30% maximum voluntary contraction. The signals were then decomposed into individual motor unit firings. We hypothesized that comparable to the upper limb, the lower limb extensor muscles (soleus) would have higher ΔF than the lower limb flexor muscles [tibialis anterior (TA)]. Contrary to our expectations, ΔF was higher in the TA than the soleus during sitting and standing despite the difference in cohort of participants and body positions. The TA also had significantly higher maximum discharge rate than the soleus while there was no difference in rate increase. When only the unit pairs with similar maximum discharge rates were compared, ∆F was still higher in the TA than the soleus. Future studies will focus on investigating the functional significance of the findings.NEW & NOTEWORTHY With the use of high-density surface array electrodes and convolutive blind source separation algorithm, thousands of motor units were decomposed from the soleus and tibialis anterior muscles. Persistent inward currents were estimated under seated and standing conditions via delta-F (∆F) calculation, and the results showed that unlike the upper limb, the flexor has higher ∆F than the extensor in the lower limb. Future studies will focus on functional significance of the findings.

Alterations in sleep, sleep spindle, and EEG power in mGluR5 knockout mice.

Abstract: Metabotropic glutamate receptor type 5 (mGluR5) knockout (KO) mice show several translationally relevant abnormalities in neural oscillatory activity associated with schizophrenia. These include de...

Population spatial frequency tuning in human early visual cortex.

Abstract: Spatial frequency selectivity is a hallmark property of early visuocortical neurons, and mapping these sensitivities gives us crucial insight into the hierarchical organization of information withi...

Amplitude modulation transfer functions reveal opposing populations within both the inferior colliculus and medial geniculate body.

Abstract: Based on single-unit recordings of modulation transfer functions (MTFs) in the inferior colliculus (IC) and the medial geniculate body (MGB) of the unanesthetized rabbit, we identified two opposing populations: band-enhanced (BE) and band-suppressed (BS) neurons. In response to amplitude-modulated (AM) sounds, firing rates of BE and BS neurons were enhanced and suppressed, respectively, relative to their responses to an unmodulated noise with a one-octave bandwidth. We also identified a third population, designated hybrid neurons, whose firing rates were enhanced by some modulation frequencies and suppressed by others. Our finding suggests that perception of AM may be based on the co-occurrence of enhancement and suppression of responses of the opposing populations of neurons. Because AM carries an important part of the content of speech, progress in understanding auditory processing of AM sounds should lead to progress in understanding speech perception. Each of the BE, BS, and hybrid types of MTFs comprised approximately one-third of the total sample. Modulation envelopes having short duty cycles of 20-50% and raised-sine envelopes accentuated the degree of enhancement and suppression and sharpened tuning of the MTFs. With sinusoidal envelopes, peak modulation frequencies were centered around 32-64 Hz among IC BE neurons, whereas the MGB peak frequencies skewed toward lower frequencies, with a median of 16 Hz. We also tested an auditory-brainstem model and found that a simple circuit containing fast excitatory synapses and slow inhibitory synapses was able to reproduce salient features of the BE- and BS-type MTFs of IC neurons.NEW & NOTEWORTHY Opposing populations of neurons have been identified in the mammalian auditory midbrain and thalamus. In response to amplitude-modulated sounds, responses of one population (band-enhanced) increased whereas responses of another (band-suppressed) decreased relative to their responses to an unmodulated sound. These opposing auditory populations are analogous to the ON and OFF populations of the visual system and may improve transfer of information carried by the temporal envelopes of complex sounds such as speech.

When 90% of the variance is not enough: residual EMG from muscle synergy extraction influences task performance

Abstract: Muscle synergies are usually identified via dimensionality reduction techniques, such that the identified synergies reconstruct the muscle activity to an accuracy level defined heuristically, often set to 90% of the variance. Here, we question the assumption that the residual muscle activity not explained by the synergies is due to noise. We hypothesize instead that the residual activity is not entirely random and can influence the execution of motor tasks. Young healthy subjects performed an isometric reaching task in which the surface electromyography of 10 arm muscles was mapped onto a two-dimensional force used to control a cursor. Three to five synergies explained 90% of the variance in muscle activity. We altered the muscle-force mapping via "hard" and "easy" virtual surgeries. Whereas in both surgeries the forces associated with synergies spanned the same dimension of the virtual environment, the muscle-force mapping was as close as possible to the initial mapping in the easy surgery; in contrast, it was as far as possible in the hard surgery. This design maximized potential differences in reaching errors attributable to residual activity. Results show that the easy surgery produced smaller directional errors than the hard surgery. Additionally, simulations of surgeries constructed with 1 to 10 synergies show that the errors in the easy and hard surgeries differ significantly for up to 8 synergies, which explains 98% of the variance on average. Our study thus indicates the need for cautious interpretations of results derived from synergy extraction techniques based on heuristics with lenient accuracy levels.NEW & NOTEWORTHY The muscle synergy hypothesis posits that the central nervous system simplifies motor control by grouping muscles into modules. Current techniques use dimensionality reduction, such that the identified synergies reconstruct 90% of the muscle activity. We show that residual muscle activity following such identification can have a large systematic effect on movements, even when the number of synergies approaches the number of muscles. Current synergy extraction techniques must therefore be updated to identify true physiological synergies.

Modulation of auditory gamma-band responses using transcranial electrical stimulation.

Abstract: Auditory gamma-band (>30 Hz) activity is a biomarker of cortical excitation/inhibition (E/I) balance in autism, schizophrenia, and bipolar disorder. We provide a comprehensive account of the effects of transcranial alternating current stimulation (tACS) and transcranial direct current stimulation (tDCS) on gamma responses. Forty-five healthy young adults listened to 40-Hz auditory click trains while electroencephalography (EEG) data were collected to measure stimulus-related gamma activity immediately before and after 10 min of 1 mA tACS (40 Hz), tDCS, or sham stimulation to left auditory cortex. tACS, but not tDCS, increased gamma power and phase locking to the auditory stimulus. However, both tACS and tDCS strengthened the gamma phase connectome, and effects persisted beyond the stimulus. Finally, tDCS strengthened the coupling of gamma activity to alpha oscillations after termination of the stimulus. No effects were observed in prestimulus gamma power, the gamma amplitude connectome, or any band-limited alpha measure. Whereas both stimulation techniques synchronize gamma responses between regions, tACS also tunes the magnitude and timing of gamma responses to the stimulus. Results reveal dissociable neurophysiological changes following tACS and tDCS and demonstrate that clinical biomarkers can be altered with noninvasive neurostimulation, especially frequency-tuned tACS.NEW & NOTEWORTHY Gamma frequency-tuned transcranial alternating current stimulation (tACS) adjusts the magnitude and timing of auditory gamma responses, as compared with both sham stimulation and transcranial direct current stimulation (tDCS). However, both tACS and tDCS strengthen the gamma phase connectome, which is disrupted in numerous neurological and psychiatric disorders. These findings reveal dissociable neurophysiological changes following two noninvasive neurostimulation techniques commonly applied in clinical and research settings.

Transcranial alternating current stimulation attenuates BOLD adaptation and increases functional connectivity.

Abstract: Concurrent transcranial alternating current stimulation (tACS) and functional MRI show that tACS affects the human brain by attenuating adaptation and increasing functional connectivity in a dose-d...