A mechanosensory feedback that uncouples external and self-generated sensory responses in the olfactory cortex.

Sampling behaviors have sensory consequences that can hinder perceptual stability. In olfaction, sniffing affects early odor encoding, mimicking a sudden change in odor concentration. We examined how the inhalation speed affects the representation of odor concentration in the main olfactory cortex. Neurons combine the odor input with a global top-down signal preceding the sniff and a mechanosensory feedback generated by the air passage through the nose during inhalation. Still, the population representation of concentration is remarkably sniff invariant. This is because the mechanosensory and olfactory responses are uncorrelated within and across neurons. Thus, faster odor inhalation and an increase in concentration change the cortical activity pattern in distinct ways. This encoding strategy affords tolerance to potential concentration fluctuations caused by varying inhalation speeds. Since mechanosensory reafferences are widespread across sensory systems, the coding scheme described here may be a canonical strategy to mitigate the sensory ambiguities caused by movements.

Living life with an electric touch.

The electric organ discharges (EODs) produced by weakly electric fish have long been a source of scientific intrigue and inspiration. The study of these species has contributed to our understanding of the organization of fixed action patterns, as well as enriching general imaging theory by unveiling the dual impact of an agent's actions on the environment and its own sensory system during the imaging process. This Centenary Review firstly compares how weakly electric fish generate species- and sex-specific stereotyped electric fields by considering: (1) peripheral mechanisms, including the geometry, channel repertoire and innervation of the electrogenic units; (2) the organization of the electric organs (EOs); and (3) neural coordination mechanisms. Secondly, the Review discusses the threefold function of the fish-centered electric fields: (1) to generate electric signals that encode the material, geometry and distance of nearby objects, serving as a short-range sensory modality or 'electric touch'; (2) to mark emitter identity and location; and (3) to convey social messages encoded in stereotypical modulations of the electric field that might be considered as species-specific communication symbols. Finally, this Review considers a range of potential research directions that are likely to be productive in the future.

Vestibular motor control.

The vestibular system is an essential sensory system that generates motor reflexes that are crucial for our daily activities, including stabilizing the visual axis of gaze and maintaining head and body posture. In addition, the vestibular system provides us with our sense of movement and orientation relative to space and serves a vital role in ensuring accurate voluntary behaviors. Neurophysiological studies have provided fundamental insights into the functional circuitry of vestibular motor pathways. A unique feature of the vestibular system compared to other sensory systems is that the same central neurons that receive direct input from the afferents of the vestibular component of the 8th nerve can also directly project to motor centers that control vital vestibular motor reflexes. In turn, these reflexes ensure stabilize gaze and the maintenance of posture during everyday activities. For instance, a direct three-neuron pathway mediates the vestibulo-ocular reflex (VOR) pathway to provide stable gaze. Furthermore, recent studies have advanced our understanding of the computations performed by the cerebellum and cortex required for motor learning, compensation, and voluntary movement and navigation. Together, these findings have provided new insights into how the brain ensures accurate self-movement during our everyday activities and have also advanced our knowledge of the neurobiological mechanisms underlying disorders of vestibular processing.

Brief Temporal Perturbations in Somatosensory Reafference Disrupt Perceptual and Neural Attenuation and Increase Supplementary Motor Area-Cerebellar Connectivity.

Intrinsic delays in sensory feedback can be detrimental for motor control. As a compensation strategy, the brain predicts the sensory consequences of movement via a forward model on the basis of a copy of the motor command. Using these predictions, the brain attenuates somatosensory reafference to facilitate the processing of exafferent information. Theoretically, this predictive attenuation is disrupted by (even minimal) temporal errors between the predicted and actual reafference; however, direct evidence of such disruption is lacking as previous neuroimaging studies contrasted nondelayed reafferent input with exafferent input. Here, we combined psychophysics with functional magnetic resonance imaging to test whether subtle perturbations in the timing of somatosensory reafference disrupt its predictive processing. Twenty-eight participants (14 women) generated touches on their left index finger by tapping a sensor with their right index finger. The touches on the left index finger were delivered close to the time of contact of the two fingers or with a temporal perturbation (i.e., 153 ms delay). We found that such a brief temporal perturbation disrupted the attenuation of the somatosensory reafference at both the perceptual and neural levels, leading to greater somatosensory and cerebellar responses and weaker somatosensory connectivity with the cerebellum, proportional to the perceptual changes. We interpret these effects as the failure of the forward model to predictively attenuate the perturbed somatosensory reafference. Moreover, we observed increased connectivity of the supplementary motor area with the cerebellum during the perturbations, which could indicate the communication of the temporal prediction error back to the motor centers.SIGNIFICANCE STATEMENT Our brain receives somatosensory feedback from our movements with a delay. To counteract these delays, motor control theories postulate that the brain predicts the timing of somatosensory consequences of our movements and attenuates sensations received at that time. Thus, a self-generated touch feels weaker than an identical external touch. However, how subtle temporal errors between the predicted and actual somatosensory feedback perturb this predictive attenuation remains unknown. We show that such errors make the otherwise attenuated touch feel stronger, elicit stronger somatosensory responses, weaken cerebellar connectivity with somatosensory areas, and increase this connectivity with motor areas. These findings show that motor and cerebellar areas are fundamental in forming temporal predictions about the sensory consequences of our movements.

The Neurobiological Basis of the Conundrum of Self-continuity: A Hypothesis.

Life, whatsoever it is, is a temporal flux. Everything is doomed to change often apparently beyond our awareness. My body appears totally different now, so does my mind. I have gained new attitudes and new ambitions, and a substantial number of old ones have been discarded. But, I am still the same person in an ongoing manner. Besides, recent neuroscientific and psychological evidence has shown that our conscious perception happens as a series of discrete or bounded instants-it emerges in temporally scattered, gappy, and discrete forms. But, if it is so, how does the brain persevere our self-continuity (or continuity of identity) in this gappy setting? How is it possible that despite moment-to-moment changes in my appearance and mind, I am still feeling that I am that person? How can we tackle with this second by second gap and resurrection in our existence which leads to a foundation of wholeness and continuity of our self? How is continuity of self (collective set of our connected experiences in the vessel of time) that results in a feeling that one's life has purpose and meaning preserved? To answer these questions, the problem has been comprehended from a philosophical, psychological, and neuroscientific perspective. I realize that first and foremost fact lies in the temporal nature of identity. Having equipped with these thoughts, in this article, it is hypothesized that according to two principles (the principle of reafference or corollary discharge and the principle of a time theory) self-continuity is maintained. It is supposed that there should be a precise temporal integration mechanism in the CNS with the outside world that provides us this smooth, ungappy flow of the Self. However, we are often taken for granted the importance of self-continuity, but it can be challenged by life transitions such as entering adulthood, retirement, senility, emigration, and societal changes such as immigration, globalization, and in much unfortunate and extreme cases of mental illnesses such as schizophrenia.

Tyraminergic corollary discharge filters reafferent perception in a chemosensory neuron.

Interpreting sensory information requires its integration with the current behavior of the animal. However, how motor-related circuits influence sensory information processing is incompletely understood. Here, we report that current locomotor state directly modulates the activity of BAG CO2 sensory neurons in Caenorhabditis elegans. By recording neuronal activity in animals freely navigating CO2 landscapes, we found that during reverse crawling states, BAG activity is suppressed by tyraminergic corollary discharge signaling. We provide genetic evidence that tyramine released from the RIM reversal interneurons extrasynaptically activates the inhibitory chloride channel LGC-55 in BAG. Disrupting this pathway genetically leads to excessive behavioral responses to CO2 stimuli. Moreover, we find that LGC-55 signaling cancels out perception of self-produced CO2 and O2 stimuli when animals reverse into their own gas plume in ethologically relevant aqueous environments. Our results show that sensorimotor integration involves corollary discharge signals directly modulating chemosensory neurons.

The Efference Copy Signal as a Key Mechanism for Consciousness.

Animals need to distinguish sensory input caused by their own movement from sensory input which is due to stimuli in the outside world. This can be done by an efference copy mechanism, a carbon copy of the movement-command that is routed to sensory structures. Here I tried to link the mechanism of the efference copy with the idea of the philosopher Thomas Reid that the senses would have a double province, to make us feel, and to make us perceive, and that, as argued by psychologist Nicholas Humphrey, the former would identify with the signals from bodily sense organs with an internalized evaluative response, i.e., with phenomenal consciousness. I discussed a possible departure from the classical implementation of the efference copy mechanism that can effectively provide the senses with such a double province, and possibly allow us some progress in understanding the nature of consciousness.

Reafference and the origin of the self in early nervous system evolution.

Discussions of the function of early nervous systems usually focus on a causal flow from sensors to effectors, by which an animal coordinates its actions with exogenous changes in its environment. We propose, instead, that much early sensing was reafferent; it was responsive to the consequences of the animal's own actions. We distinguish two general categories of reafference-translocational and deformational-and use these to survey the distribution of several often-neglected forms of sensing, including gravity sensing, flow sensing and proprioception. We discuss sensing of these kinds in sponges, ctenophores, placozoans, cnidarians and bilaterians. Reafference is ubiquitous, as ongoing action, especially whole-body motility, will almost inevitably influence the senses. Corollary discharge-a pathway or circuit by which an animal tracks its own actions and their reafferent consequences-is not a necessary feature of reafferent sensing but a later-evolving mechanism. We also argue for the importance of reafferent sensing to the evolution of the body-self, a form of organization that enables an animal to sense and act as a single unit. This article is part of the theme issue 'Basal cognition: multicellularity, neurons and the cognitive lens'.

The three second time window in poems and language processing in general: Complementarity of discrete timing and temporal continuity.

The existence of discrete time windows has triggered the search for permanence and continuity for artists (including poets) in multiple cultures throughout history. In this article, we argue that there exists a 3-s window in the temporal structure of poems as well as in the aesthetic appreciation of poetry by reviewing previous literature on the temporal aspects of poems. This 3-s window can also be considered to be a general temporal machinery underlying human behavior, including language production and perception in general. The reafference principle has provided us a unique frame for understanding cognitive processes. However, "time" was absent in the original two-stage reafference principle. Therefore, we propose a three-stage cycling model of language perception, taking into account time and time windows. We also inspect the possible neural implementations of the three stages: the generation, maintenance, and comparison of predictions (as well as the integration of predictions into the representational context). These three stages are embedded in a temporal window of ~3 s and are repeated in a cycling mode, resulting in the representational context being continuously updated. Thus, it is possible that "semantics" could be carried forward across different time windows, being a "glue" linking the discrete time windows and thus achieving the subjective feeling of temporal continuity. Candidates of such "semantic glue" could include semantic and syntactic structures as well as identity and emotion.

Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex.

Cortical development is an activity-dependent process [1-3]. Regarding the role of activity in the developing somatosensory cortex, one persistent debate concerns the importance of sensory feedback from self-generated movements. Specifically, recent studies claim that cortical activity is generated intrinsically, independent of movement [3, 4]. However, other studies claim that behavioral state moderates the relationship between movement and cortical activity [5-7]. Thus, perhaps inattention to behavioral state leads to failures to detect movement-driven activity [8]. Here, we resolve this issue by associating local field activity (i.e., spindle bursts) and unit activity in the barrel cortex of 5-day-old rats with whisker movements during wake and myoclonic twitches of the whiskers during active (REM) sleep. Barrel activity increased significantly within 500 ms of whisker movements, especially after twitches. Also, higher-amplitude movements were more likely to trigger barrel activity; when we controlled for movement amplitude, barrel activity was again greater after a twitch than a wake movement. We then inverted the analysis to assess the likelihood that increases in barrel activity were preceded within 500 ms by whisker movements: at least 55% of barrel activity was attributable to sensory feedback from whisker movements. Finally, when periods with and without movement were compared, 70%-75% of barrel activity was movement related. These results confirm the importance of sensory feedback from movements in driving activity in sensorimotor cortex and underscore the necessity of monitoring sleep-wake states to ensure accurate assessments of the contributions of the sensory periphery to activity in developing somatosensory cortex.

Visual feature tuning of superior colliculus neural reafferent responses after fixational microsaccades.

The primate superior colliculus (SC) is causally involved in microsaccade generation. Moreover, visually responsive SC neurons across this structure's topographic map, even at peripheral eccentricities much larger than the tiny microsaccade amplitudes, exhibit significant modulations of evoked response sensitivity when stimuli appear perimicrosaccadically. However, during natural viewing, visual stimuli are normally stably present in the environment and are only shifted on the retina by eye movements. Here we investigated this scenario for the case of microsaccades, asking whether and how SC neurons respond to microsaccade-induced image jitter. We recorded neural activity from two male rhesus macaque monkeys. Within the response field (RF) of a neuron, there was a stable stimulus consisting of a grating of one of three possible spatial frequencies. The grating was stable on the display, but microsaccades periodically jittered the retinotopic RF location over it. We observed clear short-latency visual reafferent responses after microsaccades. These responses were weaker, but earlier (relative to new fixation onset after microsaccade end), than responses to sudden stimulus onsets without microsaccades. The reafferent responses clearly depended on microsaccade amplitude as well as microsaccade direction relative to grating orientation. Our results indicate that one way for microsaccades to influence vision is through modulating how the spatio-temporal landscape of SC visual neural activity represents stable stimuli in the environment. Such representation depends on the specific pattern of temporal luminance modulations expected from the relative relationship between eye movement vector (size and direction) on one hand and spatial visual pattern layout on the other.NEW & NOTEWORTHY Despite being diminutive, microsaccades still jitter retinal images. We investigated how such jitter affects superior colliculus (SC) activity. We found that SC neurons exhibit short-latency visual reafferent bursts after microsaccades. These bursts reflect not only the spatial luminance profiles of visual patterns but also how such profiles are shifted by eye movement size and direction. These results indicate that the SC continuously represents visual patterns, even as they are jittered by the smallest possible saccades.

A cerebellum-like circuit in the lateral line system of fish cancels mechanosensory input associated with its own movements.

An animal's own movement exerts a profound impact on sensory input to its nervous system. Peripheral sensory receptors do not distinguish externally generated stimuli from stimuli generated by an animal's own behavior (reafference) - although the animal often must. One way that nervous systems can solve this problem is to provide movement-related signals (copies of motor commands and sensory feedback) to sensory systems, which can then be used to generate predictions that oppose or cancel out sensory responses to reafference. Here, we studied the use of movement-related signals to generate sensory predictions in the lateral line medial octavolateralis nucleus (MON) of the little skate. In the MON, mechanoreceptive afferents synapse on output neurons that also receive movement-related signals from central sources, via a granule cell parallel fiber system. This parallel fiber system organization is characteristic of a set of so-called cerebellum-like structures. Cerebellum-like structures have been shown to support predictive cancellation of reafference in the electrosensory systems of fish and the auditory system of mice. Here, we provide evidence that the parallel fiber system in the MON can generate predictions that are negative images of (and therefore cancel) sensory input associated with respiratory and fin movements. The MON, found in most aquatic vertebrates, is probably one of the most primitive cerebellum-like structures and a starting point for cerebellar evolution. The results of this study contribute to a growing body of work that uses an evolutionary perspective on the vertebrate cerebellum to understand its functional diversity in animal behavior.

Retinal Stabilization Reveals Limited Influence of Extraretinal Signals on Heading Tuning in the Medial Superior Temporal Area.

Heading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable, even though smooth-pursuit eye movements often distort optic flow. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing. Our results from 3 female monkeys demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions.SIGNIFICANCE STATEMENT Sensory systems discount stimulation caused by an animal's own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. The latter can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that extraretinal signals have little influence on activity in visual cortex, whereas visually based corrections for ongoing eye movements have stronger effects and are likely most important under real-world conditions.

Gain control in the sensorimotor system.

Coordinated movement depends on constant interaction between neural circuits that produce motor output and those that report sensory consequences. Fundamental to this process are mechanisms for controlling the influence that sensory signals have on motor pathways - for example, reducing feedback gains when they are disruptive and increasing gains when advantageous. Sensory gain control comes in many forms and serves diverse purposes - in some cases sensory input is attenuated to maintain movement stability and filter out irrelevant or self-generated signals, or enhanced to facilitate salient signals for improved movement execution and adaptation. The ubiquitous presence of sensory gain control across species at multiple levels of the nervous system reflects the importance of tuning the impact that feedback information has on behavioral output.

Corollary Discharge Signals in the Cerebellum.

The cerebellum is known to make movements fast, smooth, and accurate. Many hypotheses emphasize the role of the cerebellum in computing learned predictions important for sensorimotor calibration and feedforward control of movements. Hypotheses of the computations performed by the cerebellum in service of motor control borrow heavily from control systems theory, with models that frequently invoke copies of motor commands, called corollary discharge. This review describes evidence for corollary discharge inputs to the cerebellum and highlights the hypothesized roles for this information in cerebellar motor-related computations. Insights into the role of corollary discharge in motor control, described here, are intended to inform the exciting but still untested roles of corollary discharge in cognition, perception, and thought control relevant in psychiatric disorders.

The number-weight illusion.

When objects are manually lifted to compare their weight, then smaller objects are judged to be heavier than larger objects of the same physical weights: the classical size-weight illusion (Gregory, 2004). It is also well established that increasing numerical magnitude is strongly associated with increasing physical size: the number-size congruency effect e.g., (Besner & Coltheart Neuropsychologia, 17, 467-472 1979); Henik & Tzelgov Memory & Cognition, 10, 389-395 1982). The present study investigates the question suggested by combining these two classical effects: if smaller numbers are associated with smaller size, and objects of smaller size appear heavier, then are numbered objects (balls) of equal weight and size also judged as heavier when they carry smaller numbers? We present two experiments testing this hypothesis for weight comparisons of numbered (1 to 9) balls of equal size and weight, and report results which largely conform to an interpretation in terms of a new "number-weight illusion".

How Movement Modulates Hearing.

Hearing is often viewed as a passive process: Sound enters the ear, triggers a cascade of activity through the auditory system, and culminates in an auditory percept. In contrast to a passive process, motor-related signals strongly modulate the auditory system from the eardrum to the cortex. The motor modulation of auditory activity is most well documented during speech and other vocalizations but also can be detected during a wide variety of other sound-generating behaviors. An influential idea is that these motor-related signals suppress neural responses to predictable movement-generated sounds, thereby enhancing sensitivity to environmental sounds during movement while helping to detect errors in learned acoustic behaviors, including speech and musicianship. Findings in humans, monkeys, songbirds, and mice provide new insights into the circuits that convey motor-related signals to the auditory system, while lending support to the idea that these signals function predictively to facilitate hearing and vocal learning.

Treatment of vestibular disorders with weak asymmetric base-in prisms: An hypothesis with a focus on Ménière's disease.

BACKGROUND: Regular treatments of Ménière's disease (MD) vary largely, and no single satisfactory treatment exists. A complementary treatment popular among Dutch and Belgian patients involves eyeglasses with weak asymmetric base-in prisms, with a perceived high success rate. An explanatory mechanism is, however, lacking. OBJECTIVE: To speculate on a working mechanism explaining an effectiveness of weak asymmetric base-in prims in MD, based on available knowledge. METHODS: After describing the way these prisms are prescribed using a walking test and its effect reported on, we give an explanation of its underlying mechanism, based on the literature. RESULTS: The presumed effect can be explained by considering the typical star-like walking pattern in MD, induced by a drifting after-image comparable to the oculogyral illusion. Weak asymmetric base-in prisms can furthermore eliminate the conflict between a net vestibular angular velocity bias in the efferent signal controlling the VOR, and a net re-afferent ocular signal. CONCLUSIONS: The positive findings with these glasses reported on, the fact that the treatment itself is simple, low-cost, and socially acceptable, and the fact that an explanation is at hand, speak in favour of elaborating further on this treatment.

Towards a three-dimensional framework of centrally regulated and goal-directed exercise behaviour: a narrative review.

The Central Governor Model (CGM) ignited a paradigm shift from concepts of catastrophic failure towards central regulation of exercise performance. However, the CGM has focused on the central integration of afferent feedback in homeostatic control. Accordingly, it neglected the important role of volitional self-regulatory control and the integration of affective components inherently attached to all physiological cues. Another limitation is the large reliance on the Gestalt phenomenon of perceived exertion. Thus, progress towards a comprehensive multidimensional model of perceived fatigability and exercise regulation is needed. Drawing on Gate Control Theory of pain, we propose a three-dimensional framework of centrally regulated and goal-directed exercise behaviour, which differentiates between sensory, affective and cognitive processes shaping the perceptual milieu during exercise. We propose that: (A) perceived mental strain and perceived physical strain are primary determinants of pacing behaviour reflecting sensory-discriminatory processes necessary to align planned behaviour with current physiological state, (B) core affect plays a primary and mediatory role in exercise and performance regulation, and its underlying two dimensions hedonicity and arousal reflect affective-motivational processes triggering approach and avoidance behaviour, and (C) the mindset-shift associated with an action crisis plays a primary role in volitional self-regulatory control reflecting cognitive-evaluative processes between further goal-pursuit and goal-disengagement. The proposed framework has the potential to enrich theory development in centrally regulated and goal-directed exercise behaviour by emphasising the multidimensional dynamic processes underpinning perceived fatigability and provides a practical outline for investigating the complex interplay between the psychophysiological determinants of pacing and performance during prolonged endurance exercise.

The role of multiple internal timekeepers and sources of feedback on interval timing.

The aim of this experiment was to document the role of multiple internal clock mechanisms and external sources of temporal feedback on reducing timing variability when two fingers tap instead of one (a phenomenon known as the bimanual advantage). Previous research documents a reduction in timed interval variability when two effectors time instead of one. In addition, interval variability decreases with multiple sources of feedback. To date, however, no research has explored the separate roles of feedback and internal timing on the bimanual advantage. We evaluated the bimanual advantage in a task that does not utilise an internal clock (circle drawing). Participants performed both unimanual and bimanual timing while tapping or drawing circles. Both tasks were performed with and without tactile feedback at the timing goal. We document reduced bimanual timing variability only for tasks that utilise internal clock-like timing (tapping). We also document reduced timing variability for timing with greater sensory feedback (tactile vs no-tactile feedback tapping). We conclude that internal clock mechanisms are necessary for bimanual advantage to occur, but that multiple sources of feedback can also serve to improve internal timing, which ties together current theories of bimanual advantage.