Journal of Neurophysiology

Kass, Robert E.; Bong, Heejong; Olarinre, Motolani; Xin, Qi; Urban, Konrad N.

doi: 10.1152/jn.00131.2023pmid: 37465897

As improved recording technologies have created new opportunites for neurophysiological investigation, emphasis has shifted from individual neurons to multiple populations that form circuits, and it has become important to provide evidence of cross-population coordinated activity. We review various methods for doing so, placing them in six major categories while avoiding technical descriptions and instead focusing on high-level motivations and concerns. Our aim is to indicate what the methods can achieve and the circumstances under which they are likely to succeed. Toward this end we include discussion of four cross-cutting issues: definition of neural populations; trial-to-trial variability and Poisson-like noise; time-varying dynamics; and causality.

Kitchen, Nick M.; Yuk, Jisung; Przybyla, Andrzej; Scheidt, Robert A.; Sainburg, Robert L.

doi: 10.1152/jn.00501.2022pmid: 37529832

Prior research has shown that coordination of bilateral arm movements might be attributed to either control policies that minimize performance and control costs regardless of bilateral symmetry or by control coupling, which activates bilaterally homologous muscles as a single unit to achieve symmetric performance. We hypothesize that independent bimanual control (movements of one arm are performed without influence on the other) and co-dependent bimanual control (two arms are constrained to move together with high spatiotemporal symmetry) are two extremes on a coordination spectrum that can be negotiated to meet infinite variations in task demands. To better understand and distinguish between these views, we designed a task where minimization of either control costs or asymmetry would yield different patterns of coordination. Participants made bilateral reaches with a shared visual cursor to a midline target. We then covertly varied the gain contribution of either hand to the shared cursor's horizontal position. Across two experiments, we show that bilateral coordination retains high task-dependent sensitivity to subtle visual feedback gain asymmetries applied to the shared cursor. Specifically, we found a change from strong spatial covariation between hands during equal gains to more independent control during asymmetric gains, which occurred rapidly and with high specificity to the dimension of gain manipulation. Furthermore, the extent of spatial covariation was graded to the magnitude of perpendicular gain asymmetry between hands. These findings suggest coordination of bilateral arm movements flexibly maneuvers along a continuous coordination spectrum in a task-dependent manner that cannot be explained by bilateral control coupling.

Molle, Ludovic; Coste, Alexandre; Benoit, Charles-Etienne; Derosiere, Gerard; Janaqi, Stefan; Perrey, Stéphane; Dupeyron, Arnaud

doi: 10.1152/jn.00492.2022pmid: 37529836

The emergence of consciousness is one of biology's biggest mysteries. During the last two decades, a major effort has been made to identify the neural correlates of consciousness, but in comparison, little is known about the physiological mechanisms underlying first-person subjective experience. Attention is considered the gateway of information to consciousness. Recent work suggests that the breathing phase (i.e., inhalation versus exhalation) modulates attention, in such a way that attention directed towards exteroceptive information would increase during inhalation. One key hypothesis emerging from this work is that inhalation would improve perceptual awareness and near-threshold decision-making. The present study directly tested this hypothesis. We recorded the breathing rhythms of thirty humans performing a near-threshold decision-making task, in which they had to decide whether a liminal Gabor was tilted to the right or to the left (objective decision task) and then to rate their perceptual awareness of the Gabor orientation (subjective decision task). In line with our hypothesis, the data revealed that, relative to exhalation, inhalation improves perceptual awareness and speeds up objective decision-making, without impairing accuracy. Overall, the present study builds on timely questions regarding the physiological mechanisms underlying consciousness and shows that breathing shapes the emergence of subjective experience and decision-making.

van den Berg, Maurits M.; Busscher, Esmée; Borst, J. Gerard G.; ,

doi: 10.1152/jn.00048.2023pmid: 37465872

Amplitude modulation (AM) is a common feature of natural sounds, including speech and animal vocalizations. Here, we used operant conditioning and in vivo electrophysiology to determine the AM detection threshold of mice as well as its underlying neuronal encoding. Mice were trained in a Go-NoGo task to detect the transition to AM within a noise stimulus designed to prevent the use of spectral side-bands or a change in intensity as alternative cues. Our results indicate that mice, in comparison with other species, detect high modulation frequencies up to 512 Hz well, but show much poorer performance at low frequencies. Our in vivo multielectrode recordings in the inferior colliculus (IC) of both anesthetized and awake mice revealed a few single units with remarkable phase-locking ability to 512 Hz modulation, but not sufficient to explain the good behavioral detection at that frequency. Using a model of the population response that combined dimensionality reduction with threshold detection, we reproduced the general band-pass characteristics of behavioral detection based on a subset of neurons showing the largest firing rate change (both increase and decrease) in response to AM, suggesting that these neurons are instrumental in the behavioral detection of AM stimuli by the mice.

Guidotti, Marco; Beaurieux, Clément; Marionnaud, Pierre; Bonnet-Brilhault, Frédérique; Wardak, Claire; Latinus, Marianne

doi: 10.1152/jn.00444.2022pmid: 37492898

Objective: Somatosensory evoked potentials (SEP) studies typically characterize short latency components following median nerve stimulations of the wrist. However, these studies rarely considered 1) skin type (glabrous/hairy) at the stimulation site, 2) nerve being stimulated, and 3) middle latency (>30 ms) components. Our aim was to investigate middle latency SEPs following simple mechanical stimulation of two skin types innervated by two different nerves. Methods: 18 adults received 400 mechanical stimulations over four territories of the right hand (two nerves: radial/median; two skin types: hairy/glabrous skin) while their EEG was recorded. Results: Four middle latency components were identified: P50, N80, N130 and P200. As expected, significantly shorter latencies and larger amplitudes were found over the contralateral hemisphere for all components. A skin type effect was found for the N80: glabrous skin stimulations induced larger amplitude than hairy skin stimulations. Regarding nerve effects, median stimulations induced larger P50 and N80. Latency of the N80 was longer after median nerve stimulation compared to radial nerve stimulation. Conclusions: This study showed that skin type and stimulated nerve influence middle latency SEPs, highlighting the importance of considering these parameters in future studies. These modulations could reflect differences in cutaneous receptors and somatotopy. Middle latency SEPs can be used to evaluate the different steps of tactile information cortical processing. Significance: Modulation of SEPs components before 100 milliseconds possibly reflects somatotopy and differential processing in SI cortex.

Zhang, Yuan; Valsecchi, Matteo; Gegenfurtner, Karl R.; Chen, Jing

doi: 10.1152/jn.00469.2022pmid: 37492903

Steady-state visual evoked potentials (SSVEPs) are widely used in human neuroscience studies and applications such as brain-computer interfaces. Surprisingly, no previous study has systematically evaluated different reference methods for SSVEP analysis, despite that signal reference is crucial for the proper assessment of neural activities. In the present study, using four datasets from our previous SSVEP studies (1-3) and three public datasets from other studies (4-6), we compared four reference methods: monopolar reference, common average reference, averaged-mastoids reference, and Laplacian reference. The quality of the resulting SSVEP signals was compared in terms of both signal-to-noise ratios (SNRs) and reliability. The results showed that Laplacian reference, which uses signals at the maximally activated electrode after subtracting the average of the nearby electrodes to reduce common noise, gave rise to the highest SNRs. Furthermore, the Laplacian reference resulted in SSVEP signals that were highly reliable across recording sessions or trials. These results suggest that Laplacian reference is optimal for SSVEP studies and applications. Laplacian reference is especially advantageous for SSVEP experiments where short preparation time is preferred, since it requires only data from the maximally activated electrode and a few surrounding electrodes.

Viteri, Jose A.; Schulz, David J.

doi: 10.1152/jn.00098.2023pmid: 37529838

Recently, activity has been proposed as a primary feedback mechanism used by continuously bursting neurons to coordinate ion channel mRNA relationships that underlie stable output. However, some neuron types only have intermittent periods of activity and so may require alternative mechanisms that induce and constrain the appropriate ion channel profile in different states of activity. To address this, we used the pyloric dilator (PD; constitutively active) and the lateral gastric (LG; transiently active) neurons of the stomatogastric ganglion (STG) of the crustacean Cancer borealis. We experimentally stimulated descending inputs to the STG to cause release of neuromodulators known to elicit the active state of LG neurons and quantified the mRNA abundances and pairwise relationships of 11 voltage gated ion channels in active and silent LGs. The same stimulus does not significantly alter PD activity. Activation of LG up-regulated ion channel mRNAs and lead to a greater number of positively correlated pairwise channel mRNA relationships. Conversely, this stimulus did not induce major changes in ion channel mRNA abundances and relationships of PD cells, suggesting their ongoing activity is sufficient to maintain channel mRNA relationships even under changing modulatory conditions. Additionally, we found that ion channel mRNA correlations induced by the active state of LG are influenced by a combination of activity- and neuromodulator-dependent feedback mechanisms. Interestingly, some of these same correlations are maintained by distinct mechanisms in PD, suggesting that these motor networks utilize distinct feedback mechanisms to coordinate the same mRNA relationships across neuron types.

Missen, Kyle J.; Assländer, Lorenz; Babichuk, Alison; Chua, Romeo; Inglis, J. Timothy; Carpenter, Mark G.

doi: 10.1152/jn.00046.2023pmid: 37492897

It has been proposed that sensory force/pressure cues are integrated within a positive feedback mechanism, which accounts for the slow dynamics of human standing behaviour and helps align the body with gravity. However, experimental evidence of this mechanism remains scarce. This study tested predictions of a positive torque feedback mechanism for standing balance, specifically that differences between a "reference" torque and actual torque are self-amplified, causing the system to generate additional torque. Seventeen healthy young adults were positioned in an apparatus that permitted normal sway at the ankle until a brake on the apparatus was applied, discreetly 'locking' body movement during stance. Once locked, a platform positioned under the apparatus remained in place (0mm) or slowly translated backwards (3mm or 6mm), tilting subjects forward. Postural behaviour was characterized by two distinct responses: the centre of pressure (COP) offset (i.e., change in COP elicited by the surface translation) and the COP drift (i.e., change in COP during the sustained tilt). Model simulations were performed using a linear balance control model containing torque feedback to provide a conceptual basis for the interpretation of experimental results. Holding the body in sustained tilt positions resulted in COP drifting behaviour, reflecting attempts of the balance control system to restore an upright position through increases in plantar flexor torque. In line with predictions of positive torque feedback, larger COP offsets led to faster increases in COP over time. These findings provide experimental support for a positive torque feedback mechanism involved in the control of standing balance.

Popp, Werner L.; Richner, Lea; Lambercy, Olivier; Shirota, Camila; Barry, Alexander; Gassert, Roger; Kamper, Derek G.

doi: 10.1152/jn.00420.2020pmid: 37529845

Most of the power for generating forces in the fingers arises from muscles located in the forearm. This configuration maximizes finger joint range of range of motion while minimizing finger mass and inertia. The resulting multiarticular arrangement of the tendons, however, complicates independent control of the wrist and the digits. Actuating the wrist impacts sensorimotor control of the fingers and vice versa. The goal of this study was to systematically investigate interactions between isometric wrist and digit control. Specifically, we examined how the need to maintain a specified wrist posture influences precision grip. Fifteen healthy adults produced maximum precision grip force at 11 different wrist flexion/extension angles, with the arm was supported, under two conditions: 1) the participant maintained the desired wrist angle while performing the precision grip and 2) a robot maintained the specified wrist angle. Wrist flexion/extension posture significantly impacted maximum precision grip force (p<0.001), with the greatest grip force achieved when the wrist was extended 30° from neutral. External wrist stabilization by the robot led to a 20% increase in precision grip force across wrist postures. Increased force was accompanied by increased muscle activation, but with an activation pattern similar to the one employed when the participant had to stabilize their wrist. Thus, simultaneous wrist and finger requirements impacted performance of an isometric finger task. External wrist stabilization can promote increased precision grip force resulting from increased muscle activation. These findings have potential clinical significance for individuals with neurologically driven finger weakness, such as stroke survivors.

Nguyen, Hien; Phan, Thanh; Shadmehr, Reza; Lee, Sang Wook

doi: 10.1152/jn.00125.2023pmid: 37529847

Large bilateral asymmetry and task deficits are typically observed during bimanual actions of stroke survivors. Do these abnormalities originate from unilateral impairments affecting their more-impaired limb, e.g., weakness and abnormal synergy, or from bilateral impairments such as incoordination of two limbs? To answer this question, twenty-three subjects including ten chronic stroke survivors and thirteen neurologically-intact subjects participated in an experiment where they produced bimanual forces at different hand locations. The force magnitude and directional deviation of the more-impaired arm were measured for unilateral impairments and bimanual coordination across locations for bilateral impairments. Force asymmetry and task error were used to define task performance. Significant unilateral impairments were observed in stroke subjects; the maximal force capacity of their more-impaired arm was significantly lower than that of their less-impaired arm, with a higher degree of force deviation. However, its force contribution during submaximal tasks was greater than its relative force capacity. Significant bilateral impairments were also observed, as stroke survivors modulated two forces to a larger degree across hand locations but in a less coordinated manner than control subjects did. But only unilateral, not bilateral, impairments explained a significant amount of between-subject variability in force asymmetry across stroke subjects. Task error, in contrast, was correlated with neither unilateral nor bilateral impairments. Our results suggest that unilateral impairments of the more-impaired arm of stroke survivors mainly contribute to its reduced recruitment, but that the degree of its participation in bimanual task may be greater than their capacity as they attempt to achieve symmetry.