Psychometric Curve and Behavioral Strategies for Whisker-Based Texture Discrimination in Rats

The rodent whisker system is a major model for understanding neural mechanisms for tactile sensation of surface texture (roughness). Rats discriminate surface texture using the whiskers, and several theories exist for how texture information is physically sensed by the long, moveable macrovibrissae and encoded in spiking of neurons in somatosensory cortex. However, evaluating these theories requires a psychometric curve for texture discrimination, which is lacking. Here we trained rats to discriminate rough vs. fine sandpapers and grooved vs. smooth surfaces. Rats intermixed trials at macrovibrissa contact distance (nose >2 mm from surface) with trials at shorter distance (nose <2 mm from surface). Macrovibrissae were required for distant contact trials, while microvibrissae and non-whisker tactile cues were used for short distance trials. A psychometric curve was measured for macrovibrissa-based sandpaper texture discrimination. Rats discriminated rough P150 from smoother P180, P280, and P400 sandpaper (100, 82, 52, and 35 µm mean grit size, respectively). Use of olfactory, visual, and auditory cues was ruled out. This is the highest reported resolution for rodent texture discrimination, and constrains models of neural coding of texture information

The Advantages of a Tapered Whisker

The role of facial vibrissae (whiskers) in the behavior of terrestrial mammals is principally as a supplement or substitute for short-distance vision. Each whisker in the array functions as a mechanical transducer, conveying forces applied along the shaft to mechanoreceptors in the follicle at the whisker base. Subsequent processing of mechanoreceptor output in the trigeminal nucleus and somatosensory cortex allows high accuracy discriminations of object distance, direction, and surface texture. The whiskers of terrestrial mammals are tapered and approximately circular in cross section. We characterize the taper of whiskers in nine mammal species, measure the mechanical deflection of isolated felid whiskers, and discuss the mechanics of a single whisker under static and oscillatory deflections. We argue that a tapered whisker provides some advantages for tactile perception (as compared to a hypothetical untapered whisker), and that this may explain why the taper has been preserved during the evolution of terrestrial mammals

Functional specificity of rat vibrissal primary afferents

In this study, we propose to analyze the peripheral vibrissal system specificity through its neuronal responses. Receiver operating characteristics (ROC) curve analyses were used, which required the implementation of a binary classifier (artificial neural network) trained to identify the applied stimulus. The training phase consisted of the observation of a predetermined amount of vibrissal sweeps on two surfaces of different texture and similar roughness. Our results suggest that the specificity of the peripheral vibrissal system easily permits the discrimination between perceived stimuli, quantified through neuronal responses, and that it can be evaluated through an ROC curve analysis. We found that such specificity makes a linear binary classifier capable of detecting differences between stimuli with five sweeps at most.Fil: Lucianna, Facundo Adrián. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Farfan, Fernando Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Pizá, Alvaro Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Albarracin, Ana Lia. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; ArgentinaFil: Felice, Carmelo Jose. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentin

Active Spatial Perception in the Vibrissa Scanning Sensorimotor System

Haptic perception is an active process that provides an awareness of objects that are encountered as an organism scans its environment. In contrast to the sensation of touch produced by contact with an object, the perception of object location arises from the interpretation of tactile signals in the context of the changing configuration of the body. A discrete sensory representation and a low number of degrees of freedom in the motor plant make the ethologically prominent rat vibrissa system an ideal model for the study of the neuronal computations that underlie this perception. We found that rats with only a single vibrissa can combine touch and movement to distinguish the location of objects that vary in angle along the sweep of vibrissa motion. The patterns of this motion and of the corresponding behavioral responses show that rats can scan potential locations and decide which location contains a stimulus within 150 ms. This interval is consistent with just one to two whisk cycles and provides constraints on the underlying perceptual computation. Our data argue against strategies that do not require the integration of sensory and motor modalities. The ability to judge angular position with a single vibrissa thus connects previously described, motion-sensitive neurophysiological signals to perception in the behaving animal

Comparative study of extracellular recording methods for analysis of afferent sensory information: Empirical modeling, data analysis and interpretation

Background: Physiological studies of sensorial systems often require the acquisition and processing of data extracted from their multiple components to evaluate how the neural information changes in relation to the environment changes. In this work, a comparative study about methodological aspects of two electrophysiological approaches is described. New method: Extracellular recordings from deep vibrissal nerves were obtained by using a customized microelectrode Utah array during passive mechanical stimulation of rat´s whiskers. These recordings were compared with those obtained with bipolar electrodes. We also propose here a simplified empirical model of the electrophysiological activity obtained from a bundle of myelinated nerve fibers. Results: The peripheral activity of the vibrissal system was characterized through the temporal and spectral features obtained with both recording methods. The empirical model not only allows the correlation between anatomical structures and functional features, but also allows to predict changes in the CAPs morphology when the arrangement and the geometry of the electrodes changes. Comparison with existing method(s): This study compares two extracellular recording methods based on analysis techniques, empirical modeling and data processing of vibrissal sensory information. Conclusions: This comparative study reveals a close relationship between the electrophysiological techniques and the processing methods necessary to extract sensory information. This relationship is the result of maximizing the extraction of information from recordings of sensory activity.Fil: Farfan, Fernando Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Soto Sanchez, Cristina. Universidad de Miguel Hernández; España. Consorcio Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina; EspañaFil: Pizá, Alvaro Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Albarracin, Ana Lia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Soletta, Jorge Humberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Lucianna, Facundo Adrián. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina. Universidad Nacional de Tucumán. Facultad de Ciencias Exactas y Tecnología. Departamento de Bioingeniería. Laboratorio de Medios e Interfases; ArgentinaFil: Fernandez, Esteve. Universidad de Miguel Hernández; España. Consorcio Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina; Españ

Anatomical Pathways Involved in Generating and Sensing Rhythmic Whisker Movements

The rodent whisker system is widely used as a model system for investigating sensorimotor integration, neural mechanisms of complex cognitive tasks, neural development, and robotics. The whisker pathways to the barrel cortex have received considerable attention. However, many subcortical structures are paramount to the whisker system. They contribute to important processes, like filtering out salient features, integration with other senses, and adaptation of the whisker system to the general behavioral state of the animal. We present here an overview of the brain regions and their connections involved in the whisker system. We do not only describe the anatomy and functional roles of the cerebral cortex, but also those of subcortical structures like the striatum, superior colliculus, cerebellum, pontomedullary reticular formation, zona incerta, and anterior pretectal nucleus as well as those of level setting systems like the cholinergic, histaminergic, serotonergic, and noradrenergic pathways. We conclude by discussing how these brain regions may affect each other and how they together may control the precise timing of whisker movements and coordinate whisker perception

Perception of tactile vibrations and a putative neuronal code

We devised a delayed comparison task, appropriate for human and rats, in which subjects discriminate between pairs of vibration delivered either to their whiskers, in rats, or fingertips, in humans, with a delay inserted between the two stimuli. Stimuli were composed of a random time series of velocity values (\u201cnoise\u201d) taken from a Gaussian distribution with 0 mean and standard deviation referred to as \u3c31 for the first stimulus and \u3c32 for the second stimulus. The subject must select a response depending on the two vibrations\u2019 relative standard deviations, \u3c31>\u3c32 or \u3c31<\u3c32. In the standard condition, the base and comparison stimuli both had duration of 400 ms and they were separated by a 800 ms pause. In this condition, humans had better performance than did rats on average, yet the best rats were better than the worst humans. To learn how signals are integrated over time, we varied the duration of the second stimulus. In rats, the performance was progressively improved when the comparison stimulus duration increased from 200 to 400 and then to 600 ms. In humans, the effect of comparison stimulus duration was different: an increase in duration did not improve their performance but biased their choice. Stimuli of longer duration were perceived as having a larger value of \u3c3. We employed a novel psychophysical reverse correlation method to find out which kinematic features of the stochastic stimulus influenced the choices of the subjects. This analysis revealed that rats rely principally on features related to velocity and speed values normalized by stimulus duration \u2013 that is, the rate of velocity and speed features per unit time. In contrast, while human subjects used velocity- and speed-related features, they tended to be influenced by the summated values of those features over time. The summation strategy in humans versus the rate strategy in rats accounts for both (i) the lack of improvement in humans for greater stimulus durations and (ii) the bias by which they judged longer stimuli as having a greater value of \u3c3. Next, we focused on the capacity of rats to accomplish a task of parametric working memory, a capacity until now not found in rodents. For delays between the base and comparison stimuli of up to 6-10 seconds, humans and rats showed similar performance. However when the difference in \u3c3 was small, the rats\u2019 performance began to decay over long inter-stimulus delays more markedly than did the humans\u2019 performance. The next chapter reports the analyses of the activity of barrel cortex neurons during the vibration comparison task. 35% of sampled neuron clusters showed a significant change in firing rate as \u3c3 varied, and the change was positive in every case \u2013 the slope of firing rate versus \u3c3 was positive. We used methods related to signal detection theory to estimate the behavioral performance that could be supported by single neuron clusters and found that the resulting \u201cneurometric\u201d curve was much less steep performance than the psychometric curve (the performance of the whole rat). This led to the notion that stimuli are encoded by larger populations. A general linear model (GLM) that combined multiple simultaneously recorded 2 clusters performed much better than single clusters and began to approach animal performance. We conclude that a potential code for the stimulus is the variation in firing rate according to \u3c3, distributed across large populations.In conclusion, this thesis characterizes the perceptual capacities of humans and rats in a novel working memory task. Both humans and rats can extract the statistical structure of a \u201cnoisy\u201d tactile vibration, but seem to integrate signals by different operations. A major finding is that rats are endowed with a capacity to hold stimulus parameters in working memory with a proficiency that, until now, could be ascribed only to primates. The statistical properties of the stimulus appear to be encoded by a distributed population

Active touch sensing in pinnipeds

Active touch sensing in humans is characterised by making purposive movements with their fingertips. These movements are task-specific to maximise the relevant information gathered from an object. In whisker-touch sensing, previous research has suggested that whisker movements are purposive, but no one has ever examined task-specific whisker movements in any animal. Pinnipeds are whisker specialists, with long, mobile, sensitive whiskers and diverse whisker morphologies. The aim of this PhD is to investigate active touch sensing in Pinnipeds (seals, sea lions and walrus), by: i) describing whisker morphology; ii) comparing and quantifying whisker movements; and iii) characterising task-dependency of whisker movements during texture, size and luminance discrimination tasks. Pinnipeds with long, numerous whiskers, such as California sea lions (Zalophus californianus) and Stellar sea lions (Eumetopias jubatus) have larger infraorbital foramen (IOF) sizes and therefore, more sensitive whiskers. The IOF being a small hole in the skull, allowing the infraorbital nerve (ION) to pass through, which supplies sensation to the whiskers. Comparing whisker movements in Harbor seals (Phoca vitulina), California sea lions and Pacific walrus (Odobenidae rosmarus), showed these species all protracted their whiskers forwards and oriented their head towards a moving fish stimulus. However, California sea lions moved their whiskers more than the other species, and independently of the head. Due to the movement capabilities and sensitivity of whiskers in California sea lions, this species was used to investigate whether whiskers can be moved in a task-specific way. Results suggested that California sea lions make task-specific movements, by feeling around the edge of different-sized shapes, and focussing and spreading their whiskers on the centre of different-textured shapes. Therefore, California sea lion whiskers are controlled like a true active touch sensory system, similar to human fingertips. I suggest that active touch sensing is likely to efficiently guide foraging and prey capture in dark, murky waters in these animals. Moreover, the complexity of California sea lion whisker movements and their subsequent behaviours makes them a good candidate from which to further investigate animal decision-making, perception and cognition

Tactile cognition in rodents

Since the discovery 50 years ago of the precisely ordered representation of the whiskers in somatosensory cortex, the rodent tactile sensory system has been a fertile ground for the study of sensory processing. With the growing sophistication of touch-based behavioral paradigms, together with advances in neurophysiological methodology, a new approach is emerging. By posing increasingly complex perceptual and memory problems, in many cases analogous to human psychophysical tasks, investigators now explore the operations underlying rodent problem solving. We define the neural basis of tactile cognition as the transformation from a stage in which neuronal activity encodes elemental features, local in space and in time, to a stage in which neuronal activity is an explicit representation of the behavioral operations underlying the current task. Selecting a set of whisker-based behavioral tasks, we show that rodents achieve high level performance through the workings of neuronal cir-cuits that are accessible, decodable, and manipulatable. As a means towards exploring tactile cognition, this review presents leading psychophysical paradigms and, where known, their neural correlates