Inter-participant consistency of language-processing networks during abstract thoughts.

Human brain imaging typically employs structured and controlled tasks to avoid variable and inconsistent activation patterns. Here we expand this assumption by showing that an extremely open-ended, high-level cognitive task of thinking about an abstract content, loosely defined as "abstract thinking" - leads to highly consistent activation maps. Specifically, we show that activation maps generated during such cognitive process were precisely located relative to borders of well-known networks such as internal speech, visual and motor imagery. The activation patterns allowed decoding the thought condition at >95%. Surprisingly, the activated networks remained the same regardless of changes in thought content. Finally, we found remarkably consistent activation maps across individuals engaged in abstract thinking. This activation bordered, but strictly avoided visual and motor networks. On the other hand, it overlapped with left lateralized language networks. Activation of the default mode network (DMN) during abstract thought was similar to DMN activation during rest. These observations were supported by a quantitative neuronal distance metric analysis. Our results reveal that despite its high level, and varied content nature - abstract thinking activates surprisingly precise and consistent networks in participants' brains.

Alpha and beta band event-related desynchronization reflects kinematic regularities.

The short-lasting attenuation of brain oscillations is termed event-related desynchronization (ERD). It is frequently found in the alpha and beta bands in humans during generation, observation, and imagery of movement and is considered to reflect cortical motor activity and action-perception coupling. The shared information driving ERD in all these motor-related behaviors is unknown. We investigated whether particular laws governing production and perception of curved movement may account for the attenuation of alpha and beta rhythms. Human movement appears to be governed by relatively few kinematic laws of motion. One dominant law in biological motion kinematics is the 2/3 power law (PL), which imposes a strong dependency of movement speed on curvature and is prominent in action-perception coupling. Here we directly examined whether the 2/3 PL elicits ERD during motion observation by characterizing the spatiotemporal signature of ERD. ERDs were measured while human subjects observed a cloud of dots moving along elliptical trajectories either complying with or violating the 2/3 PL. We found that ERD within both frequency bands was consistently stronger, arose faster, and was more widespread while observing motion obeying the 2/3 PL. An activity pattern showing clear 2/3 PL preference and lying within the alpha band was observed exclusively above central motor areas, whereas 2/3 PL preference in the beta band was observed in additional prefrontal-central cortical sites. Our findings reveal that compliance with the 2/3 PL is sufficient to elicit a selective ERD response in the human brain.

Alterations in task-induced activity and resting-state fluctuations in visual and DMN areas revealed in long-term meditators.

Recently we proposed that the information contained in spontaneously emerging (resting-state) fluctuations may reflect individually unique neuro-cognitive traits. One prediction of this conjecture, termed the "spontaneous trait reactivation" (STR) hypothesis, is that resting-state activity patterns could be diagnostic of unique personalities, talents and life-styles of individuals. Long-term meditators could provide a unique experimental group to test this hypothesis. Using fMRI we found that, during resting-state, the amplitude of spontaneous fluctuations in long-term mindfulness meditation (MM) practitioners was enhanced in the visual cortex and significantly reduced in the DMN compared to naïve controls. Importantly, during a visual recognition memory task, the MM group showed heightened visual cortex responsivity, concomitant with weaker negative responses in Default Mode Network (DMN) areas. This effect was also reflected in the behavioral performance, where MM practitioners performed significantly faster than the control group. Thus, our results uncover opposite changes in the visual and default mode systems in long-term meditators which are revealed during both rest and task. The results support the STR hypothesis and extend it to the domain of local changes in the magnitude of the spontaneous fluctuations.

Motor-sensory confluence in tactile perception.

Perception involves motor control of sensory organs. However, the dynamics underlying emergence of perception from motor-sensory interactions are not yet known. Two extreme possibilities are as follows: (1) motor and sensory signals interact within an open-loop scheme in which motor signals determine sensory sampling but are not affected by sensory processing and (2) motor and sensory signals are affected by each other within a closed-loop scheme. We studied the scheme of motor-sensory interactions in humans using a novel object localization task that enabled monitoring the relevant overt motor and sensory variables. We found that motor variables were dynamically controlled within each perceptual trial, such that they gradually converged to steady values. Training on this task resulted in improvement in perceptual acuity, which was achieved solely by changes in motor variables, without any change in the acuity of sensory readout. The within-trial dynamics is captured by a hierarchical closed-loop model in which lower loops actively maintain constant sensory coding, and higher loops maintain constant sensory update flow. These findings demonstrate interchangeability of motor and sensory variables in perception, motor convergence during perception, and a consistent hierarchical closed-loop perceptual model.

Idiosyncratic selection of active touch for shape perception.

Hand movements are essential for tactile perception of objects. However, the specific functions served by active touch strategies, and their dependence on physiological parameters, are unclear and understudied. Focusing on planar shape perception, we tracked at high resolution the hands of 11 participants during shape recognition task. Two dominant hand movement strategies were identified: contour following and scanning. Contour following movements were either tangential to the contour or oscillating perpendicular to it. Scanning movements crossed between distant parts of the shapes' contour. Both strategies exhibited non-uniform coverage of the shapes' contours. Idiosyncratic movement patterns were specific to the sensed object. In a second experiment, we have measured the participants' spatial and temporal tactile thresholds. Significant portions of the variations in hand speed and in oscillation patterns could be explained by the idiosyncratic thresholds. Using data-driven simulations, we show how specific strategy choices may affect receptors activation. These results suggest that motion strategies of active touch adapt to both the sensed object and to the perceiver's physiological parameters.

Invariance of firing rate and field potential dynamics to stimulus modulation rate in human auditory cortex.

The effect of stimulus modulation rate on the underlying neural activity in human auditory cortex is not clear. Human studies (using both invasive and noninvasive techniques) have demonstrated that at the population level, auditory cortex follows stimulus envelope. Here we examined the effect of stimulus modulation rate by using a rare opportunity to record both spiking activity and local field potentials (LFP) in auditory cortex of patients during repeated presentations of an audio-visual movie clip presented at normal, double, and quadruple speeds. Mean firing rate during evoked activity remained the same across speeds and the temporal response profile of firing rate modulations at increased stimulus speeds was a linearly scaled version of the response during slower speeds. Additionally, stimulus induced power modulation of local field potentials in the high gamma band (64-128 Hz) exhibited similar temporal scaling as the neuronal firing rate modulations. Our data confirm and extend previous studies in humans and anesthetized animals, supporting a model in which both firing rate, and high-gamma LFP power modulations in auditory cortex follow the temporal envelope of the stimulus across different modulation rates.

Active sensory substitution allows fast learning via effective motor-sensory strategies.

We examined the development of new sensing abilities in adults by training participants to perceive remote objects through their fingers. Using an Active-Sensing based sensory Substitution device (ASenSub), participants quickly learned to perceive fast via the new modality and preserved their high performance for more than 20 months. Both sighted and blind participants exhibited almost complete transfer of performance from 2D images to novel 3D physical objects. Perceptual accuracy and speed using the ASenSub were, on average, 300% and 600% better than previous reports for 2D images and 3D objects. This improvement is attributed to the ability of the participants to employ their own motor-sensory strategies. Sighted participants dominant strategy was based on motor-sensory convergence on the most informative regions of objects, similarly to fixation patterns in vision. Congenitally, blind participants did not show such a tendency, and many of their exploratory procedures resembled those observed with natural touch.

Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations.

BACKGROUND: To what extent is activity of individual neurons coupled to the local field potential (LFP) and to blood-oxygenation-level dependent (BOLD) functional magnetic resonance imaging (fMRI)? This issue is of high significance for understanding brain function and for relating animal studies to fMRI, yet it is still under debate. RESULTS: Here we report data from simultaneous recordings of isolated unit activity and LFP by using multiple electrodes in the human auditory cortex. We found a wide range of coupling levels between the activity of individual neurons and gamma LFP. However, this large variability could be predominantly explained (r = 0.66) by the degree of firing-rate correlations between neighboring neurons. Importantly, this phenomenon occurred during both sensory stimulation and spontaneous activity. Concerning the coupling of neuronal activity to BOLD fMRI, we found that gamma LFP was well coupled to BOLD measured across different individuals (r = 0.62). By contrast, the coupling of single units to BOLD was highly variable and, again, tightly related to interneuronal-firing-rate correlations (r = 0.70). CONCLUSIONS: Our results offer a resolution to a central controversy regarding the coupling between neurons, LFP, and BOLD signals by demonstrating, for the first time, that the coupling of single units to the other measures is variable yet it is tightly related to the degree of interneuronal correlations in the human auditory cortex.

Spontaneously emerging cortical representations of visual attributes.

Spontaneous cortical activity--ongoing activity in the absence of intentional sensory input--has been studied extensively, using methods ranging from EEG (electroencephalography), through voltage sensitive dye imaging, down to recordings from single neurons. Ongoing cortical activity has been shown to play a critical role in development, and must also be essential for processing sensory perception, because it modulates stimulus-evoked activity, and is correlated with behaviour. Yet its role in the processing of external information and its relationship to internal representations of sensory attributes remains unknown. Using voltage sensitive dye imaging, we previously established a close link between ongoing activity in the visual cortex of anaesthetized cats and the spontaneous firing of a single neuron. Here we report that such activity encompasses a set of dynamically switching cortical states, many of which correspond closely to orientation maps. When such an orientation state emerged spontaneously, it spanned several hypercolumns and was often followed by a state corresponding to a proximal orientation. We suggest that dynamically switching cortical states could represent the brain's internal context, and therefore reflect or influence memory, perception and behaviour.

Motion-induced blindness and microsaccades: cause and effect.

It has been suggested that subjective disappearance of visual stimuli results from a spontaneous reduction of microsaccade rate causing image stabilization, enhanced adaptation, and a consequent fading. In motion-induced blindness (MIB), salient visual targets disappear intermittently when surrounded by a moving pattern. We investigated whether changes in microsaccade rate can account for MIB. We first determined that the moving mask does not affect microsaccade metrics (rate, magnitude, and temporal distribution). We then compared the dynamics of microsaccades during reported illusory disappearance (MIB) and physical disappearance (Replay) of a salient peripheral target. We found large modulations of microsaccade rate following perceptual transitions, whether illusory (MIB) or real (Replay). For MIB, the rate also decreased prior to disappearance and increased prior to reappearance. Importantly, MIB persisted in the presence of microsaccades although sustained microsaccade rate was lower during invisible than visible periods. These results suggest that the microsaccade system reacts to changes in visibility, but microsaccades also modulate MIB. The latter modulation is well described by a Poisson model of the perceptual transitions assuming that the probability for reappearance and disappearance is modulated following a microsaccade. Our results show that microsaccades counteract disappearance but are neither necessary nor sufficient to account for MIB.

Early-vision brain responses which predict human visual segmentation and learning.

Brain processes underlying visual segmentation have been widely studied, being part of the basic processes underlying perception. However, the underlying constraints on perceptual thresholds, set by neuronal processing, remain unclear. Here, the relationship between human visual performance and brain activity was examined using the backward-masked texture segmentation task. Performance showed dependence on the time-interval between target and mask as well as on the amount of prior practice. Correspondingly, early components of human event-related potentials (ERPs) recorded over occipital electrodes showed strong interactions between target and mask responses, suggesting interference with perception processes when the presented mask interacts with sustained target processing. These interactions, revealing an otherwise undetected extended processing time course beyond the early component of the target response, enabled us to quantify individual neuronal thresholds that closely matched the behavioral thresholds (r = 0.93, p = 0.00003). Furthermore, these neuronal thresholds could be improved by practice, suggesting neuronal mechanisms affected by perceptual learning. Predicting performance level not directly detected in the ERP but rather by further interactions shown here in early stages of the visual hierarchy may have important implications in the study of human perception. Practice seems to reduce the temporal interactions between the successive stimuli, revealing brain processes underlying perceptual learning.

Layer-specific touch-dependent facilitation and depression in the somatosensory cortex during active whisking.

Brains adapt to new situations by retuning their neurons. The most common form of neuronal adaptation, typically observed with repetitive stimulations of passive sensory organs, is depression (responses gradually decrease until stabilized). We studied cortical adaptation when stimuli are acquired by active movements of the sensory organ. In anesthetized rats, artificial whisking was induced at 5 Hz, and activity of individual neurons in layers 2-5 was recorded during whisking in air (Whisking condition) and whisking against an object (Touch condition). Response strengths were assessed by spike counts. Input-layer responses (layers 4 and 5a) usually facilitated during the whisking train, whereas superficial responses (layer 2/3) usually depressed. In layers 2/3 and 4, but not 5a, responses were usually stronger during touch trials than during whisking in air. Facilitations were specific to the protraction phase; during retraction, responses depressed in all layers and conditions. These dynamic processes were accompanied by a slow positive wave of activity progressing from superficial to deeper layers and lasting for approximately 1 s, during the transient phase of response. Our results indicate that, in the cortex, adaptation does not depend only on the level of activity or the frequency of its repetition but rather on the nature of the sensory information that is conveyed by that activity and on the processing layer. The input and laminar specificities observed here are consistent with the hypothesis that the paralemniscal layer 5a is involved in the processing of whisker motion, whereas the lemniscal barrels in layer 4 are involved in the processing of object identity.

Active construction of percepts about object location.

Mammals acquire much of their sensory information by actively moving their sensory organs. Rats, in particular, scan their surrounding environment with their whiskers. This form of active sensing induces specific patterns of temporal encoding of sensory information, which are based on a conversion of space into time via sensor movement. We investigate the ways in which object location is encoded by the whiskers and decoded by the brain. We recorded from first-order neurons located in the trigeminal ganglion (TG) of anaesthetized rats during epochs of artificial whisking induced by electrical stimulation of the facial motor nerve. We found that TG neurons encode the three positional coordinates with different codes. The horizontal coordinate (along the backward-forward axis) is encoded by two encoding schemes, both relying on the firing times of one type of TG neuron, the 'contact cell'. The radial coordinate (from face outward) is encoded primarily by the firing magnitude of another type of TG neurons, the 'pressure cell'. The vertical coordinate (from ground up) is encoded by the identity of activated neurons. The decoding schemes of at least some of these sensory cues, our data suggest, are also active: cortical representations are generated by a thalamic comparison of cortical expectations with incoming sensory data.

On the possible roles of microsaccades and drifts in visual perception.

During natural viewing large saccades shift the visual gaze from one target to another every few hundreds of milliseconds. The role of microsaccades (MSs), small saccades that show up during long fixations, is still debated. A major debate is whether MSs are used to redirect the visual gaze to a new location or to encode visual information through their movement. We argue that these two functions cannot be optimized simultaneously and present several pieces of evidence suggesting that MSs redirect the visual gaze and that the visual details are sampled and encoded by ocular drifts. We show that drift movements are indeed suitable for visual encoding. Yet, it is not clear to what extent drift movements are controlled by the visual system, and to what extent they interact with saccadic movements. We analyze several possible control schemes for saccadic and drift movements and propose experiments that can discriminate between them. We present the results of preliminary analyses of existing data as a sanity check to the testability of our predictions.

Data for default network reduced functional connectivity in meditators, negatively correlated with meditation expertise.

FMRI data described here was recorded during resting-state in Mindfulness Meditators (MM) and control participants (see "Task-induced activity and resting-state fluctuations undergo similar alterations in visual and DMN areas of long-term meditators" Berkovich-Ohana et al. (2016) [1] for details). MM participants were also scanned during meditation. Analyses focused on functional connectivity within and between the default mode network (DMN) and visual network (Vis). Here we show data demonstrating that: 1) Functional connectivity within the DMN and the Visual networks were higher in the control group than in the meditators; 2) Data show an increase for the functional connectivity between the DMN and the Visual networks in the meditators compared to controls; 3) Data demonstrate that functional connectivity both within and between networks reduces during meditation, compared to the resting-state; and 4) A significant negative correlation was found between DMN functional connectivity and meditation expertise. The reader is referred to Berkovich-Ohana et al. (2016) [1] for further interpretation and discussion.

Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex.

Sensory processing and its perception require that local information would also be available globally. Indeed, in the mammalian neocortex, local excitation spreads over large distances via the long-range horizontal connections in layer 2/3 and may spread over an entire cortical area if excitatory polysynaptic pathways are also activated. Therefore, a balance between local excitation and surround inhibition is required. Here we explore the spatiotemporal aspects of cortical depolarization and hyperpolarization of rats anesthetized with urethane. New voltage-sensitive dyes (VSDs) were used for high-resolution real-time visualization of the cortical responses to whisker deflections and cutaneous stimulations of the whisker pad. These advances facilitated imaging of ongoing activity and evoked responses even without signal averaging. We found that the motion of a single whisker evoked a cortical response exhibiting either one or three phases. During a triphasic response, there was first a cortical depolarization in a small cortical region the size of a single cortical barrel. Subsequently, this depolarization increased and spread laterally in an oval manner, preferentially along rows of the barrel field. During the second phase, the amplitude of the evoked response declined rapidly, presumably because of recurrent inhibition. Subsequently, the third phase exhibiting a depolarization rebound was observed and clear, and approximately 16 Hz oscillations were detected. Stimulus conditions revealing a net surround hyperpolarization during the second phase were also found. By using new, improved VSD, the present findings shed new light on the spatial parameters of the intricate spatiotemporal cortical interplay of inhibition and excitation.

1-D Vision: Encoding of Eye Movements by Simple Receptive Fields.

Eye movements (eyeM) are an essential component of visual perception. They allow the sampling and scanning of stationary scenes at various spatial scales, primarily at the scene level, via saccades, and at the local level, via fixational eyeM. Given the constant motion of visual images on the retina, a crucial factor in resolving spatial ambiguities related to the external scene is the exact trajectory of eyeM. We show here that the trajectory of eyeM can be encoded at high resolution by simple retinal receptive fields of the symmetrical type. We also show that such encoding can account for motion illusions such as the Ouchi illusion. In addition, encoding of motion projections along horizontal and vertical symmetrical simple retinal receptive fields entails a kind of Cartesian decomposition of the 2-D image into two 1-D projections.

Repetitive speech elicits widespread deactivation in the human cortex: the "Mantra" effect?

BACKGROUND: Mantra (prolonged repetitive verbal utterance) is one of the most universal mental practices in human culture. However, the underlying neuronal mechanisms that may explain its powerful emotional and cognitive impact are unknown. In order to try to isolate the effect of silent repetitive speech, which is used in most commonly practiced Mantra meditative practices, on brain activity, we studied the neuronal correlates of simple repetitive speech in nonmeditators - that is, silent repetitive speech devoid of the wider context and spiritual orientations of commonly practiced meditation practices. METHODS: We compared, using blood oxygenated level-dependent (BOLD) functional magnetic resonance imaging (fMRI), a simple task of covertly repeating a single word to resting state activity, in 23 subjects, none of which practiced meditation before. RESULTS: We demonstrate that the repetitive speech was sufficient to induce a widespread reduction in BOLD signal compared to resting baseline. The reduction was centered mainly on the default mode network, associated with intrinsic, self-related processes. Importantly, contrary to most cognitive tasks, where cortical-reduced activation in one set of networks is typically complemented by positive BOLD activity of similar magnitude in other cortical networks, the repetitive speech practice resulted in unidirectional negative activity without significant concomitant positive BOLD. A subsequent behavioral study showed a significant reduction in intrinsic thought processes during the repetitive speech condition compared to rest. CONCLUSIONS: Our results are compatible with a global gating model that can exert a widespread induction of negative BOLD in the absence of a corresponding positive activation. The triggering of a global inhibition by the minimally demanding repetitive speech may account for the long-established psychological calming effect associated with commonly practiced Mantra-related meditative practices.

Optical imaging combined with targeted electrical recordings, microstimulation, or tracer injections.

To facilitate the combination of optical imaging with various electrode-based techniques, we have designed and produced a skull-mounting "sliding-top cranial window" and a removable "electrode positioner microdrive". These new devices were used to study sensory processing in chronic and acute experiments in the cerebral cortices of cats and monkeys. This assembly allows simultaneous optical imaging of intrinsic signals or voltage-sensitive dyes combined with extracellular recording (single and multiple unit recording and local field potential), intracellular recording, microstimulation, or targeted injection of tracers. After the functional architecture is determined by optical imaging, electrodes are targeted into a selected cortical site under full visual control, at a variety of penetration angles (30-90 degrees ), accessing a large cortical area. The device consists of three parts: (1) a skull-mounting chamber, (2) a sliding cap, and (3) a microdrive. The microdrive can easily be removed and the cranial window is then sealed and covered with a flat protective cover. For chronic experiments, this arrangement allows the animal to be handled over a long period while fitted with a sealed cranial window of minimal volume and weight, and with negligible risk of accidental damage or infection.