Co-coding of head and whisker movements by both VPM and POm thalamic neurons.

Rodents continuously move their heads and whiskers in a coordinated manner while perceiving objects through whisker-touch. Studies in head-fixed rodents showed that the ventroposterior medial (VPM) and posterior medial (POm) thalamic nuclei code for whisker kinematics, with POm involvement reduced in awake animals. To examine VPM and POm involvement in coding head and whisker kinematics in awake, head-free conditions, we recorded thalamic neuronal activity and tracked head and whisker movements in male mice exploring an open arena. Using optogenetic tagging, we found that in freely moving mice, both nuclei equally coded whisker kinematics and robustly coded head kinematics. The fraction of neurons coding head kinematics increased after whisker trimming, ruling out whisker-mediated coding. Optogenetic activation of thalamic neurons evoked overt kinematic changes and increased the fraction of neurons leading changes in head kinematics. Our data suggest that VPM and POm integrate head and whisker information and can influence head kinematics during tactile perception.

Functional anatomy of mystacial active sensing in rats.

Rats' whisking motion and objects' palpation produce tactile signals sensed by mechanoreceptors at the vibrissal follicles. Rats adjust their whisking patterns to target information type, flow, and resolution, adapting to their behavioral needs and the changing environment. This coordination requires control over the activity of the mystacial pad's intrinsic and extrinsic muscles. Studies have relied on muscle recording and stimulation techniques to describe the roles of individual muscles. However, these methods lack the resolution to isolate the mystacial pad's small and compactly arranged muscles. Thus, we propose functional anatomy as a complementary approach for studying the individual and coordinated effects of the mystacial pad muscles on vibrissae movements. Our functional analysis addresses the kinematic measurements of whisking motion patterns recorded in freely exploring rats. Combined with anatomical descriptions of muscles and fascia elements of the mystacial pad in situ, we found: (1) the contributions of individual mystacial pad muscles to the different whisking motion patterns; (2) active touch by microvibrissae, and its underlying mechanism; and (3) dynamic position changes of the vibrissae pivot point, as determined by the movements of the corium and subcapsular fibrous mat. Finally, we hypothesize that each of the rat mystacial pad muscles is specialized for a particular function in a way that matches the architecture of the fascial structures. Consistent with biotensegrity principles, the muscles and fascia form a network of structural support and continuous tension that determine the arrangement and motion of the embedded individual follicles.

Thalamocortical loops as temporal demodulators across senses.

Sensory information is coded in space and in time. The organization of neuronal activity in space maintains straightforward relationships with the spatial organization of the perceived environment. In contrast, the temporal organization of neuronal activity is not trivially related to external features due to sensor motion. Still, the temporal organization shares similar principles across sensory modalities. Likewise, thalamocortical circuits exhibit common features across senses. Focusing on touch, vision, and audition, we review their shared coding principles and suggest that thalamocortical systems include circuits that allow analogous recoding mechanisms in all three senses. These thalamocortical circuits constitute oscillations-based phase-locked loops, that translate temporally-coded sensory information to rate-coded cortical signals, signals that can integrate information across sensory and motor modalities. The loop also allows predictive locking to the onset of future modulations of the sensory signal. The paper thus suggests a theoretical framework in which a common thalamocortical mechanism implements temporal demodulation across senses.

Inferring visual space from ultra-fine extra-retinal knowledge of gaze position.

It has long been debated how humans resolve fine details and perceive a stable visual world despite the incessant fixational motion of their eyes. Current theories assume these processes to rely solely on the visual input to the retina, without contributions from motor and/or proprioceptive sources. Here we show that contrary to this widespread assumption, the visual system has access to high-resolution extra-retinal knowledge of fixational eye motion and uses it to deduce spatial relations. Building on recent advances in gaze-contingent display control, we created a spatial discrimination task in which the stimulus configuration was entirely determined by oculomotor activity. Our results show that humans correctly infer geometrical relations in the absence of spatial information on the retina and accurately combine high-resolution extraretinal monitoring of gaze displacement with retinal signals. These findings reveal a sensory-motor strategy for encoding space, in which fine oculomotor knowledge is used to interpret the fixational input to the retina.

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.

Time in the brain: Encoding does not mean perceiving.

The neural basis of time perception remains an enigma. In rats performing interval judgment tasks, striatal time coding has drawn attention as one potential substrate. Toso et al. (2021b) find that such time coding does not account for stimulus duration perception.

Oculo-retinal dynamics can explain the perception of minimal recognizable configurations.

Natural vision is a dynamic and continuous process. Under natural conditions, visual object recognition typically involves continuous interactions between ocular motion and visual contrasts, resulting in dynamic retinal activations. In order to identify the dynamic variables that participate in this process and are relevant for image recognition, we used a set of images that are just above and below the human recognition threshold and whose recognition typically requires >2 s of viewing. We recorded eye movements of participants while attempting to recognize these images within trials lasting 3 s. We then assessed the activation dynamics of retinal ganglion cells resulting from ocular dynamics using a computational model. We found that while the saccadic rate was similar between recognized and unrecognized trials, the fixational ocular speed was significantly larger for unrecognized trials. Interestingly, however, retinal activation level was significantly lower during these unrecognized trials. We used retinal activation patterns and oculomotor parameters of each fixation to train a binary classifier, classifying recognized from unrecognized trials. Only retinal activation patterns could predict recognition, reaching 80% correct classifications on the fourth fixation (on average, ∼2.5 s from trial onset). We thus conclude that the information that is relevant for visual perception is embedded in the dynamic interactions between the oculomotor sequence and the image. Hence, our results suggest that ocular dynamics play an important role in recognition and that understanding the dynamics of retinal activation is crucial for understanding natural vision.

Interactions of Whisking and Touch Signals in the Rat Brainstem.

Perception is an active process, requiring the integration of both proprioceptive and exteroceptive information. In the rat's vibrissal system, a classical model for active sensing, the relative contribution of the two information streams was previously studied at the peripheral, thalamic, and cortical levels. Contributions of brainstem neurons were only indirectly inferred for some trigeminal nuclei according to their thalamic projections. The current work addressed this knowledge gap by performing the first comparative study of the encoding of proprioceptive whisking and exteroceptive touch signals in the oralis (SpVo), interpolaris (SpVi), and paratrigeminal (Pa5) brainstem nuclei. We used artificial whisking in anesthetized male rats, which allows a systematic analysis of the relative contribution of the proprioceptive and exteroceptive information streams along the ascending pathways in the absence of motor or cognitive top-down modulations. We found that (1) neurons in the rostral and caudal parts of the SpVi convey whisking and touch information, respectively, as predicted by their thalamic projections; (2) neurons in the SpVo encode both whisking and (primarily) touch information; and (3) neurons of the Pa5 encode a complex combination of whisking and touch information. In particular, the Pa5 contains a relatively large fraction of neurons that are inhibited by active touch, a response observed so far only in the thalamus. Overall, our systematic characterization of afferent responses to active touch in the trigeminal brainstem approves the hypothesized functions of SpVi neurons and presents evidence that SpVo and Pa5 neurons are involved in the processing of active vibrissal touch.SIGNIFICANCE STATEMENT The present work constitutes the first comparative study of the encoding of proprioceptive (whisking) and exteroceptive (touch) information in the rat's brainstem trigeminal nuclei, the first stage of vibrissal processing in the CNS. It shows that (1) as expected, the rostral and caudal interpolaris neurons convey primarily whisking and touch information, respectively; (2) the oralis nucleus, whose function was previously unknown, encodes both whisking and (primarily) touch touch information; (3) a subtractive computation, reported at the thalamic level, already occurs at the brainstem level; and (4) a novel afferent pathway probably ascends via the paratrigeminal nucleus, encoding both proprioceptive and exteroceptive information.

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.

Interaction between muscles and fascia in the mystacial pad of whisking rodents.

In whisking rodents, the mystacial pad is supplied with vibrissae and contains a collagenous skeleton that is a part of the snout fascia. The collagenous skeleton is composed of three interconnected layers: superficial, deep spongy mesh and subcapsular fibrous mat. We found that the first two layers contain diverse fascial structures, such as sheets of subcutaneous connective tissue, tendons, ligaments and follicular capsules which transmit muscle efforts to vibrissae and are thus involved in whisking. Subcapsular fibrous mat is built of oriented rostro-caudal wavy fibrils. It maintains spatial arrangement of whisker follicles, provides a quick response to deformation and connects entire mystacial pad to the skull. To move vibrissae, the forces of intrinsic muscles are applied directly to the capsules of the vibrissa follicles, whereas the forces of extrinsic muscles are applied to other parts of the collagenous skeleton, which transmit the forces to the capsules. According to the spatial distribution and anchoring sites of the muscles and fascia, extrinsic muscles provide vibrissa protraction or retraction by pulling the superficial layer of the collagenous skeleton rostral or caudal, respectively. Vibrissae can be also retracted when the efforts of extrinsic muscles are applied to the subcapsular fibrous mat. When the muscles relax, fascial structures return the vibrissae to their resting position. The deep spongy layer encompasses vibrissal follicles providing a uniform distribution of stresses and strains during whisking. In the mystacial pad, fascia is a dominant type of tissue that maintains the integrity of the vibrissa motor plant, translates muscular momentum to the vibrissae, and plays a role in vibrissae movements.

Closed loop motor-sensory dynamics in human vision.

Vision is obtained with a continuous motion of the eyes. The kinematic analysis of eye motion, during any visual or ocular task, typically reveals two (kinematic) components: saccades, which quickly replace the visual content in the retinal fovea, and drifts, which slowly scan the image after each saccade. While the saccadic exchange of regions of interest (ROIs) is commonly considered to be included in motor-sensory closed-loops, it is commonly assumed that drifts function in an open-loop manner, that is, independent of the concurrent visual input. Accordingly, visual perception is assumed to be based on a sequence of open-loop processes, each initiated by a saccade-triggered retinal snapshot. Here we directly challenged this assumption by testing the dependency of drift kinematics on concurrent visual inputs using real-time gaze-contingent-display. Our results demonstrate a dependency of the trajectory on the concurrent visual input, convergence of speed to condition-specific values and maintenance of selected drift-related motor-sensory controlled variables, all strongly indicative of drifts being included in a closed-loop brain-world process, and thus suggesting that vision is inherently a closed-loop process.

Predictive whisker kinematics reveal context-dependent sensorimotor strategies.

Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such as mice and rats, employ cyclic scanning motions of their facial whiskers to explore their proximal surrounding, a behavior known as whisking. Here, we investigated the contingency of whisking kinematics on the animal's behavioral context that arises from both internal processes (attention and expectations) and external constraints (available sensory and motor degrees of freedom). We recorded rat whisking at high temporal resolution in 2 experimental contexts-freely moving or head-fixed-and 2 spatial sensory configurations-a single row or 3 caudal whiskers on each side of the snout. We found that rapid sensorimotor twitches, called pumps, occurring during free-air whisking carry information about the rat's upcoming exploratory direction, as demonstrated by the ability of these pumps to predict consequent head and body locomotion. Specifically, pump behavior during both voluntary motionlessness and imposed head fixation exposed a backward redistribution of sensorimotor exploratory resources. Further, head-fixed rats employed a wide range of whisking profiles to compensate for the loss of head- and body-motor degrees of freedom. Finally, changing the number of intact vibrissae available to a rat resulted in an alteration of whisking strategy consistent with the rat actively reallocating its remaining resources. In sum, this work shows that rats adapt their active exploratory behavior in a homeostatic attempt to preserve sensorimotor coverage under changing environmental conditions and changing sensory capacities, including those imposed by various laboratory conditions.

Generalization of Object Localization From Whiskers to Other Body Parts in Freely Moving Rats.

Rats can be trained to associate relative spatial locations of objects with the spatial location of rewards. Here we ask whether rats can localize static silent objects with other body parts in the dark, and if so with what resolution. We addressed these questions in trained rats, whose interactions with the objects were tracked at high-resolution before and after whisker trimming. We found that rats can use other body parts, such as trunk and ears, to localize objects. Localization resolution with non-whisking body parts (henceforth, 'body') was poorer than that obtained with whiskers, even when left with a single whisker at each side. Part of the superiority of whiskers was obtained via the use of multiple contacts. Transfer from whisker to body localization occurred within one session, provided that body contacts with the objects occurred before whisker trimming, or in the next session otherwise. This transfer occurred whether temporal cues were used for discrimination or when discrimination was based on spatial cues alone. Rats' decision in each trial was based on the sensory cues acquired in that trial and on decisions and reward locations in previous trials. When sensory cues were acquired by body contacts, rat decisions relied more on the reward location in previous trials. Overall, the results suggest that rats can generalize the idea of relative object location across different body parts, while preferring to rely on whiskers-based localization, which occurs earlier and conveys higher resolution.

Temporal Coding of Visual Space.

Establishing a representation of space is a major goal of sensory systems. Spatial information, however, is not always explicit in the incoming sensory signals. In most modalities it needs to be actively extracted from cues embedded in the temporal flow of receptor activation. Vision, on the other hand, starts with a sophisticated optical imaging system that explicitly preserves spatial information on the retina. This may lead to the assumption that vision is predominantly a spatial process: all that is needed is to transmit the retinal image to the cortex, like uploading a digital photograph, to establish a spatial map of the world. However, this deceptively simple analogy is inconsistent with theoretical models and experiments that study visual processing in the context of normal motor behavior. We argue here that, as with other senses, vision relies heavily on temporal strategies and temporal neural codes to extract and represent spatial information.

A self-adjusting head holder without ear-bars for guinea pigs.

A self-adjusting head holder is designed to allow stable fixation and precise positioning (anterior-posterior, pitch, and roll) of guinea pig head in stereotaxic devices. These are achieved with no use of ear-bars. It is thus easy to use, preferable for studies of the auditory system, and for avoiding tissue damage of the ear in general. This head holder can accommodate various head sizes and is thus adapted for males and females of a large range of body weights, as confirmed for guinea pigs of 360-940 g. Moreover, this head holder is easy and cost-effective to manufacture, making it accessible for any lab. Here, we present background and mechanical rationale, the technical specifications, and step-by-step manufacturing instructions for the stainless-steel and the plastic MRI-compatible versions of our self-adjusting head holder.

Building Bridges through Science.

Science is ideally suited to connect people from different cultures and thereby foster mutual understanding. To promote international life science collaboration, we have launched "The Science Bridge" initiative. Our current project focuses on partnership between Western and Middle Eastern neuroscience communities.

Attention Robustly Gates a Closed-Loop Touch Reflex.

Rats' large whiskers (macrovibrissae) are used to explore their nearby environment, typically using repetitive protraction-retraction "whisking" motions that are coordinated with head and body movements [1-8]. Once objects are detected, the rat can further explore the object tactually by using both the macrovibrissae and an array of shorter, stationary microvibrissae on the chin, as well as by using the lips [9-11]. When touch occurs during whisking, a fast reflexive response, termed a touch-induced pump (TIP), may be triggered. During a TIP, the whisker slightly retracts and protracts again, doubling the number of pressure onsets per contact. In head-fixed rats, TIPs occur in ∼25% of the contacts [12]. Here we report that the occurrence of TIPs depends strongly on attention, indicated by head-turning toward an object: when rats intended to explore an object, either after encountering it during free exploration or when expecting its existence, the probability of a TIP increased from <30% to >65% without an increase in TIP latency. TIP regulation was unilateral and specific to the attended object; when two objects were palpated bilaterally simultaneously, TIP probability increased to >65% and decreased to <20% for contacts with the apparently-attended and apparently-unattended object, respectively. A data-driven computational model indicates that attentional gating could not be triggered by object contact, due to temporal constraints; rather, it could be based on a normally enabled or whisking-triggered scheme. Taken together, our results suggest that object-related attention regulates contact dynamics by gating the operation of a brainstem motor-sensory-motor loop and that this regulation is optimized for fast reaction.

Muscular Basis of Whisker Torsion in Mice and Rats.

Whisking mammals move their whiskers in the rostrocaudal and dorsoventral directions with simultaneous rolling about their long axes (torsion). Whereas muscular control of the first two types of whisker movement was already established, the anatomic muscular substrate of the whisker torsion remains unclear. Specifically, it was not clear whether torsion is induced by asymmetrical operation of known muscles or by other largely unknown muscles. Here, we report that mystacial pads of newborn and adult rats and mice contain oblique intrinsic muscles (OMs) that connect diagonally adjacent vibrissa follicles. Each of the OMs is supplied by a cluster of motor end plates. In rows A and B, OMs connect the ventral part of the rostral follicle with the dorsal part of the caudal follicle. In rows C-E, in contrast, OMs connect the dorsal part of the rostral follicle to the ventral part of the caudal follicle. This inverse architecture is consistent with previous behavioral observations [Knutsen et al.: Neuron 59 (2008) 35-42]. In newborn mice, torsion occurred in irregular single twitches. In adult anesthetized rats, microelectrode mediated electrical stimulation of an individual OM that is coupled with two adjacent whiskers was sufficient to induce a unidirectional torsion of both whiskers. Torsional movement was associated with protracting movement, indicating that in the vibrissal system, like in the ocular system, torsional movement is mechanically coupled to horizontal and vertical movements. This study shows that torsional whisker rotation is mediated by specific OMs whose morphology and attachment sites determine rotation direction and mechanical coupling, and motor innervation determines rotation dynamics. Anat Rec, 300:1643-1653, 2017. © 2017 Wiley Periodicals, Inc.

What Do Sensory Organs Tell the Brain?

Understanding how perception emerges depends on the understanding of sensory acquisition by sensory organs. In this issue of Neuron, Severson et al. (2017) present a brilliant leap towards understanding active sensory coding by mechanoreceptors.

Perception as a closed-loop convergence process.

Perception of external objects involves sensory acquisition via the relevant sensory organs. A widely-accepted assumption is that the sensory organ is the first station in a serial chain of processing circuits leading to an internal circuit in which a percept emerges. This open-loop scheme, in which the interaction between the sensory organ and the environment is not affected by its concurrent downstream neuronal processing, is strongly challenged by behavioral and anatomical data. We present here a hypothesis in which the perception of external objects is a closed-loop dynamical process encompassing loops that integrate the organism and its environment and converging towards organism-environment steady-states. We discuss the consistency of closed-loop perception (CLP) with empirical data and show that it can be synthesized in a robotic setup. Testable predictions are proposed for empirical distinction between open and closed loop schemes of perception.