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.

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.

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.

Motion makes sense: an adaptive motor-sensory strategy underlies the perception of object location in rats.

Tactile perception is obtained by coordinated motor-sensory processes. We studied the processes underlying the perception of object location in freely moving rats. We trained rats to identify the relative location of two vertical poles placed in front of them and measured at high resolution the motor and sensory variables (19 and 2 variables, respectively) associated with this whiskers-based perceptual process. We found that the rats developed stereotypic head and whisker movements to solve this task, in a manner that can be described by several distinct behavioral phases. During two of these phases, the rats' whiskers coded object position by first temporal and then angular coding schemes. We then introduced wind (in two opposite directions) and remeasured their perceptual performance and motor-sensory variables. Our rats continued to perceive object location in a consistent manner under wind perturbations while maintaining all behavioral phases and relatively constant sensory coding. Constant sensory coding was achieved by keeping one group of motor variables (the "controlled variables") constant, despite the perturbing wind, at the cost of strongly modulating another group of motor variables (the "modulated variables"). The controlled variables included coding-relevant variables, such as head azimuth and whisker velocity. These results indicate that consistent perception of location in the rat is obtained actively, via a selective control of perception-relevant motor variables.

Thalamic relay or cortico-thalamic processing? Old question, new answers.

What are the functions implemented by neurons in the sensory nuclei of the thalamus? It seems that this question has accompanied cortical and thalamic studies since their onset some 6 decades ago. Over the years, the simplistic, traditional view of thalamic neurons as mere relays of sensory information has given way to more sophisticated views, of which several alternative hypotheses have been proposed. This commentary briefly reviews the 2 current major hypotheses and shows how a new, pioneering experiment, published in Cerebral Cortex by Groh, Acsady and colleagues, discriminates between them. The commentary further elaborates on the thalamo-cortical processing suggested by the new findings, the general sensory-motor scheme to which these findings may be relevant, and the possible roles such thalamo-cortical processing may have in sensory-motor control.

Coding of object location in the vibrissal thalamocortical system.

In whisking rodents, object location is encoded at the receptor level by a combination of motor and sensory related signals. Recoding of the encoded signals can result in various forms of internal representations. Here, we examined the coding schemes occurring at the first forebrain level that receives inputs necessary for generating such internal representations--the thalamocortical network. Single units were recorded in 8 thalamic and cortical stations in artificially whisking anesthetized rats. Neuronal representations of object location generated across these stations and expressed in response latency and magnitude were classified based on graded and binary coding schemes. Both graded and binary coding schemes occurred across the entire thalamocortical network, with a general tendency of graded-to-binary transformation from thalamus to cortex. Overall, 63% of the neurons of the thalamocortical network coded object position in their firing. Thalamocortical responses exhibited a slow dynamics during which the amount of coded information increased across 4-5 whisking cycles and then stabilized. Taken together, the results indicate that the thalamocortical network contains dynamic mechanisms that can converge over time on multiple coding schemes of object location, schemes which essentially transform temporal coding to rate coding and gradual to labeled-line coding.

Emergent exploration via novelty management.

When encountering novel environments, animals perform complex yet structured exploratory behaviors. Despite their typical structuring, the principles underlying exploratory patterns are still not sufficiently understood. Here we analyzed exploratory behavioral data from two modalities: whisking and locomotion in rats and mice. We found that these rodents maximized novelty signal-to-noise ratio during each exploration episode, where novelty is defined as the accumulated information gain. We further found that these rodents maximized novelty during outbound exploration, used novelty-triggered withdrawal-like retreat behavior, and explored the environment in a novelty-descending sequence. We applied a hierarchical curiosity model, which incorporates these principles, to both modalities. We show that the model captures the major components of exploratory behavior in multiple timescales: single excursions, exploratory episodes, and developmental timeline. The model predicted that novelty is managed across exploratory modalities. Using a novel experimental setup in which mice encountered a novel object for the first time in their life, we tested and validated this prediction. Further predictions, related to the development of brain circuitry, are described. This study demonstrates that rodents select exploratory actions according to a novelty management framework and suggests a plausible mechanism by which mammalian exploration primitives can be learned during development and integrated in adult exploration of complex environments.

Structure-function correlations of rat trigeminal primary neurons: Emphasis on club-like endings, a vibrissal mechanoreceptor.

This study focuses on the structure and function of the primary sensory neurons that innervate vibrissal follicles in the rat. Both the peripheral and central terminations, as well as their firing properties were identified using intracellular labelling and recording in trigeminal ganglia in vivo. Fifty-one labelled neurons terminating peripherally, as club-like, Merkel, lanceolate, reticular or spiny endings were identified by their morphology. All neurons responded robustly to air puff stimulation applied to the vibrissal skin. Neurons with club-like endings responded with the highest firing rates; their peripheral processes rarely branched between the cell body and their terminal tips. The central branches of these neurons displayed abundant collaterals terminating within all trigeminal nuclei. Analyses of three-dimensional reconstructions reveal a palisade arrangement of club-like endings bound to the ringwulst by collagen fibers. Our morphological findings suggest that neurons with club-like endings sense mechanical aspects related to the movement of the ringwulst and convey this information to all trigeminal nuclei in the brainstem.

Learning and control of exploration primitives.

Animals explore novel environments in a cautious manner, exhibiting alternation between curiosity-driven behavior and retreats. We present a detailed formal framework for exploration behavior, which generates behavior that maintains a constant level of novelty. Similar to other types of complex behaviors, the resulting exploratory behavior is composed of exploration motor primitives. These primitives can be learned during a developmental period, wherein the agent experiences repeated interactions with environments that share common traits, thus allowing transference of motor learning to novel environments. The emergence of exploration motor primitives is the result of reinforcement learning in which information gain serves as intrinsic reward. Furthermore, actors and critics are local and ego-centric, thus enabling transference to other environments. Novelty control, i.e. the principle which governs the maintenance of constant novelty, is implemented by a central action-selection mechanism, which switches between the emergent exploration primitives and a retreat policy, based on the currently-experienced novelty. The framework has only a few parameters, wherein time-scales, learning rates and thresholds are adaptive, and can thus be easily applied to many scenarios. We implement it by modeling the rodent's whisking system and show that it can explain characteristic observed behaviors. A detailed discussion of the framework's merits and flaws, as compared to other related models, concludes the paper.

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.

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.

'Where' and 'what' in the whisker sensorimotor system.

In the visual system of primates, different neuronal pathways are specialized for processing information about the spatial coordinates of objects and their identity - that is, 'where' and 'what'. By contrast, rats and other nocturnal animals build up a neuronal representation of 'where' and 'what' by seeking out and palpating objects with their whiskers. We present recent evidence about how the brain constructs a representation of the surrounding world through whisker-mediated sense of touch. While considerable knowledge exists about the representation of the physical properties of stimuli - like texture, shape and position - we know little about how the brain represents their meaning. Future research may elucidate this and show how the transformation of one representation to another is achieved.

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.

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.

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.

When outgoing and incoming signals meet: new insights from the zona incerta.

In the sense of touch, it is the motion of the sensory receptors themselves that leads to an afferent signal-whether these receptors are in our fingertips sliding along a surface or a rat's whiskers palpating an object. Afferent signals can be correctly interpreted only if the sensory system receives information about the brain's own motor output. In this issue of Neuron, Urbain and Deschênes provide new insights into the physiological and anatomical interplay between tactile and motor signals in rats.

Temporal and spatial characteristics of vibrissa responses to motor commands.

A mechanistic description of the generation of whisker movements is essential for understanding the control of whisking and vibrissal active touch. We explore how facial-motoneuron spikes are translated, via an intrinsic muscle, to whisker movements. This is achieved by constructing, simulating, and analyzing a computational, biomechanical model of the motor plant, and by measuring spiking to movement transformations at small and large angles using high-precision whisker tracking in vivo. Our measurements revealed a supralinear summation of whisker protraction angles in response to consecutive motoneuron spikes with moderate interspike intervals (5 ms < Deltat < 30 ms). This behavior is explained by a nonlinear transformation from intracellular changes in Ca(2+) concentration to muscle force. Our model predicts the following spatial constraints: (1) Contraction of a single intrinsic muscle results in movement of its two attached whiskers with different amplitudes; the relative amplitudes depend on the resting angles and on the attachment location of the intrinsic muscle on the anterior whisker. Counterintuitively, for a certain range of resting angles, activation of a single intrinsic muscle can lead to a retraction of one of its two attached whiskers. (2) When a whisker is pulled by its two adjacent muscles with similar forces, the protraction amplitude depends only weakly on the resting angle. (3) Contractions of two adjacent muscles sums up linearly for small amplitudes and supralinearly for larger amplitudes. The model provides a direct translation from motoneuron spikes to whisker movements and can serve as a building block in closed-loop motor-sensory models of active touch.

Orthogonal coding of object location.

It has been argued whether internal representations are encoded using a universal ('the neural code') or multiple codes. Here, we review a series of experiments that demonstrate that tactile encoding of object location via whisking employs an orthogonal, triple-code scheme. Rats, and other rodents, actively move the whiskers back and forth to localize and identify objects. Neural recordings from primary sensory afferents, along with behavioral observations, demonstrate that vertical coordinates of contacted objects are encoded by the identity of activated afferents, horizontal coordinates by the timing of activation and radial coordinates by the intensity of activation. Because these codes are mutually independent, the three-dimensional location of an object could, in principle, be encoded by individual afferents during single whisker-object contacts. One advantage of such a same-neuron-different-codes scheme over the traditionally assumed same-code-different-neurons scheme is a reduction of code ambiguity that, in turn, simplifies decoding circuits.

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.