scholarly journals Spontaneous neural oscillations influence behavior and sensory representations by suppressing neuronal excitability

Author(s):  
Luca Iemi ◽  
Laura Gwilliams ◽  
Jason Samaha ◽  
Ryszard Auksztulewicz ◽  
Yael M Cycowicz ◽  
...  

AbstractThe ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Spontaneous fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on invasive electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.

2018 ◽  
Author(s):  
Luca Iemi ◽  
Niko A Busch ◽  
Annamaria Laudini ◽  
Saskia Haegens ◽  
Jason Samaha ◽  
...  

AbstractSpontaneous fluctuations of neural activity may explain why sensory responses vary across repeated presentations of the same physical stimulus. To test this hypothesis, we recorded electroencephalography in humans during stimulation with identical visual stimuli and analyzed how prestimulus neural oscillations modulate different stages of sensory processing reflected by distinct components of the event-related potential (ERP). We found that strong prestimulus alpha- and beta-band power resulted in a suppression of early ERP components (C1 and N150) and in an amplification of late components (after 0.4 s), even after controlling for fluctuations in 1/f aperiodic signal and sleepiness. Whereas functional inhibition of sensory processing underlies the reduction of early ERP responses, we found that the modulation of non-zero-mean oscillations (baseline shift) accounted for the amplification of late responses. Distinguishing between these two mechanisms is crucial for understanding how internal brain states modulate the processing of incoming sensory information.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Luca Iemi ◽  
Niko A Busch ◽  
Annamaria Laudini ◽  
Saskia Haegens ◽  
Jason Samaha ◽  
...  

Spontaneous fluctuations of neural activity may explain why sensory responses vary across repeated presentations of the same physical stimulus. To test this hypothesis, we recorded electroencephalography in humans during stimulation with identical visual stimuli and analyzed how prestimulus neural oscillations modulate different stages of sensory processing reflected by distinct components of the event-related potential (ERP). We found that strong prestimulus alpha- and beta-band power resulted in a suppression of early ERP components (C1 and N150) and in an amplification of late components (after 0.4 s), even after controlling for fluctuations in 1/f aperiodic signal and sleepiness. Whereas functional inhibition of sensory processing underlies the reduction of early ERP responses, we found that the modulation of non-zero-mean oscillations (baseline shift) accounted for the amplification of late responses. Distinguishing between these two mechanisms is crucial for understanding how internal brain states modulate the processing of incoming sensory information.


2020 ◽  
Vol 45 (9) ◽  
pp. 845-854
Author(s):  
Nicholas Fallon ◽  
Timo Giesbrecht ◽  
Anna Thomas ◽  
Andrej Stancak

Abstract Congruent visual cues augment sensitivity to brief olfactory presentations and habituation of odor perception is modulated by central-cognitive processing including context. However, it is not known whether habituation to odors could interact with cross-modal congruent stimuli. The present research investigated the effect of visual congruence on odor detection sensitivity during continuous odor exposures. We utilized a multimethod approach, including subjective behavioral responses and reaction times (RTs; study 1) and electroencephalography (EEG, study 2). Study 1: 25 participants received 2-min presentations of moderate-intensity floral odor delivered via olfactometer with congruent (flower) and incongruent (object) image presentations. Participants indicated odor perception after each image. Detection sensitivity and RTs were analyzed in epochs covering the period of habituation. Study 2: 25 new participants underwent EEG recordings during 145-s blocks of odor presentations with congruent or incongruent images. Participants passively observed images and intermittently rated the perceived intensity of odor. Event-related potential analysis was utilized to evaluate brain processing related to odor–visual pairs across the period of habituation. Odor detection sensitivity and RTs were improved by congruent visual cues. Results highlighted a diminishing influence of visual congruence on odor detection sensitivity as habituation occurred. Event-related potential analysis revealed an effect of congruency on electrophysiological processing in the N400 component. This was only evident in early periods of odor exposure when perception was strong. For the first time, this demonstrates the modulation of central processing of odor–visual pairs by habituation. Frontal negativity (N400) responses encode the aspects of cross-modal congruence for odor–vision cross-modal tasks.


Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 137-137
Author(s):  
W H Ehrenstein ◽  
J Lewald ◽  
L Schlykowa

We asked to what extent the respective gaze direction influences (i) the spatial congruence of perceived direction of auditory and visual cues, and (ii) the discrimination of the direction of target motion. With fixed head position, subjects directed their gaze in various positions and localised auditory targets (band-pass noise, 2 kHz) presented at one of nine positions (straight ahead, or four symmetric positions to the left or right separated by 2.75 deg, respectively). Forced-choice judgements, whether the sound was perceived to the left or right of a visual reference light, show that the azimuth of the sound was perceived as slightly shifted to the left of a visual reference when the gaze was directed to the left, and vice versa. The maximum of this relative auditory - visual shift was 4.7 deg over a range of 45 deg (left or right) of gaze directions. In (ii), a spot of light started at the centre of a monitor and moved at 2 or 12 deg s−1 leftward or rightward. Subjects reported the direction by pressing a key; their gaze was directed at 0, 8, or 16 deg to the left or right. Mean choice-reaction times increased with increasing gaze eccentricity, but differently depending on stimulus direction and speed: with left fixation they were shorter for leftward than rightward motion; with right fixation they were shorter for rightward motion. This effect was stronger for the slow than for the fast stimulus speed. Thus, facilitation occurs when stimuli move with moderate velocity toward the direction of gaze. While the auditory-visual shift in (i) may reflect an incomplete transformation of spatial (craniocentric and oculocentric) coordinates as suggested by recordings in the primate midbrain, the results in (ii) conform with reports of specialised units in the posterior parietal cortex (areas LIP, 7a, MST) that, in registering oculomotor position, modulate visual sensitivity.


1969 ◽  
Vol 29 (1) ◽  
pp. 23-33 ◽  
Author(s):  
Kenneth Gaarder

The general systems model of central sensory processing used in this study is based on the assumption that central processing is discontinuous and raises this question: Is concurrent processing of different sense modalities serial, parallel, or independent? Since an eye-jump indicates input of visual information, if the auditory system is stimulated by clicks with fixed delays after eye-jumps, intermodality relationships are tested. Reaction times and evoked responses show complex interactions which are interpreted to suggest serial processing analogous to time sharing computers.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Tal Golan ◽  
Ido Davidesco ◽  
Meir Meshulam ◽  
David M Groppe ◽  
Pierre Mégevand ◽  
...  

A key hallmark of visual perceptual awareness is robustness to instabilities arising from unnoticeable eye and eyelid movements. In previous human intracranial (iEEG) work (Golan et al., 2016) we found that excitatory broadband high-frequency activity transients, driven by eye blinks, are suppressed in higher-level but not early visual cortex. Here, we utilized the broad anatomical coverage of iEEG recordings in 12 eye-tracked neurosurgical patients to test whether a similar stabilizing mechanism operates following small saccades. We compared saccades (1.3°−3.7°) initiated during inspection of large individual visual objects with similarly-sized external stimulus displacements. Early visual cortex sites responded with positive transients to both conditions. In contrast, in both dorsal and ventral higher-level sites the response to saccades (but not to external displacements) was suppressed. These findings indicate that early visual cortex is highly unstable compared to higher-level visual regions which apparently constitute the main target of stabilizing extra-retinal oculomotor influences.


2020 ◽  
Author(s):  
Zachary Davis ◽  
Gabriel Benigno ◽  
Charlee Fletterman ◽  
Theo Desbordes ◽  
Terrence Sejnowski ◽  
...  

Abstract Sensory neuroscience has focused a great deal of its attention on characterizing the mean firing rate that is evoked by a stimulus, and while it has long been recognized that the firing rates of individual neurons fluctuate around the mean, these fluctuations are often treated as a form of internally generated noise1. There is, however, evidence that these “ongoing” fluctuations of activity in sensory cortex during normal, waking function shape neuronal excitability and responses to external input2,3. We have recently found that spontaneous fluctuations are organized into waves traveling at speeds consistent with the speed of action potentials traversing unmyelinated horizontal cortical fibers (0.1-0.6 m/s)4 across the cortical surface5. These waves systematically modulate excitability across the retinotopic map, strongly affecting perceptual sensitivity as measured in a visual detection task. The underlying mechanism for these waves, however, is unknown. Further, it is unclear whether waves are consistent with the low rate, highly irregular, and weakly correlated “asynchronous-irregular” dynamics observed in computational models6 and cortical recordings in vivo7. Here, we study a large-scale computational model of a cortical sheet, with connections ranging up to biological scales. Using an efficient custom simulation framework, we study networks with topographically-organized connectivity and distance-dependent axonal conduction delays from several thousand up to one million neurons. We find that spontaneous traveling waves are a general property of these networks and are consistent with the asynchronous-irregular regime. These waves are well matched to spontaneous waves recorded in the neocortex of awake monkeys. Further, individual neurons sparsely participate in waves, yielding a sparse-wave regime that offers a unique operating mode, where traveling waves coexist with locally asynchronous-irregular dynamics, without inducing deleterious neuronal correlations8.


2019 ◽  
Author(s):  
Zachary W. Davis ◽  
Lyle Muller ◽  
Julio-Martinez Trujillo ◽  
Terrence Sejnowski ◽  
John H. Reynolds

AbstractPerceptual sensitivity varies from moment to moment. One potential source of variability is spontaneous fluctuations in cortical activity that can travel as a wave. Spontaneous traveling waves have been reported during anesthesia, but questioned as to whether they are relevant to waking cortical function. Using newly developed analytic techniques, we find spontaneous waves of activity in extrastriate visual cortex of awake marmosets (Callithrix jacchus). In monkeys trained to detect faint visual targets, the timing and position of spontaneous traveling waves, prior to target onset, predict the magnitude of evoked activity and the likelihood of detection. In contrast, spatially disorganized fluctuations of neural activity are much less predictive. These results reveal an important role for spontaneous traveling waves in sensory processing through modulating neural and perceptual sensitivity.One Sentence SummaryFluctuations in cortical activity often travel as waves, shape incoming sensory information, and affect conscious perception.


Author(s):  
Sture Hansson

The function of sleep in mammal and other vertebrates is one of the great mysteries of biology. Many hypotheses have been proposed, but few of these have made even the slightest attempt to explain the essence of sleep - the uncompromising need for reversible unconsciousness. During sleep, epiphenomena - often of a somatic character - occur, but these cannot explain the core function of sleep. One answer could be hidden in the observations made for long periods of time of the function of the central nervous system (CNS). The CNS is faced with conflicting requirements on stability and excitability. A high level of excitability is desirable, and is also a prerequisite for sensitivity and quick reaction times; however, it can also lead to instability and the risk of feedback, with life-threatening epileptic seizures. Activity-dependent negative feedback in neuronal excitability improves stability in the short term, but not to the degree that is required. A hypothesis is presented here demonstrating how calibration of individual neurons - an activity which occurs only during sleep - can establish the balanced and highest possible excitability while also preserving stability in the CNS. One example of a possible mechanism is the observation of slow oscillations in EEGs made on birds and mammals during slow wave sleep. Calibration to a genetically determined level of excitability could take place in individual neurons during the slow oscillation, so that action potentials are generated during the oscillations “up-phase”. This can only take place offline, which explains the need for sleep. The hypothesis can explain phenomena such as the need for unconsciousness during sleep, with the disconnection of sensory stimuli, slow EEG oscillations, the relationship of sleep and epilepsy, age, the effects of sleep on neuronal firing rate and the effects of sleep deprivation and sleep homeostasis. This is with regard primarily to mammals, including humans, but also all other vertebrates.


NeuroImage ◽  
2021 ◽  
pp. 118746
Author(s):  
Luca Iemi ◽  
Laura Gwilliams ◽  
Jason Samaha ◽  
Ryszard Auksztulewicz ◽  
Yael M Cycowicz ◽  
...  

Sign in / Sign up

Export Citation Format

Share Document