RESUMEN

Rodents rely on their whiskers as vital sensory tools for tactile perception, enabling them to distinguish textures and shapes. Ensuring the reliability and constancy of tactile perception under varying stimulus conditions remains a fascinating and fundamental inquiry. This study explores the impact of stimulus configurations, including whisker movement velocity and object spatial proximity, on texture discrimination and stability in rats. To address this issue, we employed three distinct approaches for our investigation. Stimulus configurations notably affected tactile inputs, altering whisker vibration's kinetic and kinematic aspects with consistent effects across various textures. Through a texture discrimination task, rats exhibited consistent discrimination performance irrespective of changes in stimulus configuration. However, alterations in stimulus configuration significantly affected the rats' ability to maintain stability in texture perception. Additionally, we investigated the influence of stimulus configurations on cortical neuronal responses by manipulating them experimentally. Notably, cortical neurons demonstrated substantial and intricate changes in firing rates without compromising the ability to discriminate between textures. Nevertheless, these changes resulted in a reduction in texture neuronal response stability. Stimulating multiple whiskers led to improved neuronal texture discrimination and maintained coding stability. These findings emphasize the importance of considering numerous factors and their interactions when studying the impact of stimulus configuration on neuronal responses and behavior.

RESUMEN

During tactile sensation in rodents, the whisker movements across surfaces give rise to intricate whisker motions that encompass discrete and transient stick-slip events, effectively conveying valuable information regarding surface properties. These surface characteristics are transformed into cortical neuronal responses. This study examined the coding strategies underlying these transformations in rat whiskers. We found that changes in surface coarseness modified the number and magnitude of stick-slip events, which in turn both modulated properties of neuronal responses. Global changes in the number of stick-slip events primarily affected neuronal discharge rates and the degree of neuronal synchronization. In contrast, local changes in the magnitude of stick-slip events affected the transformation of these kinematic and kinetic characteristics into neuronal discharges. Most cortical neurons exhibited surface coarseness selectivity through global and local stick-slip event properties. However, this selectivity varied across coding strategies in the same neurons, given that each coding strategy reflected different aspects of changes in whisker-surface interactions. The degree of spatial similarity in surface coarseness preference in adjacently recorded neurons differed among these coding strategies. Adjacently recorded neurons exhibited the same surface coarseness preference in their firing rates but not through other coding strategies. Through these results, we were able to show that local stick-slip event properties contribute to texture discrimination, complementing and surpassing global coding in this context. These findings suggest that the representation of surface coarseness in the cortex may rely on concurrent coding strategies that integrate tactile information across different spatiotemporal scales.

RESUMEN

During tactile sensation by rodents, whisker movements across surfaces generate complex whisker motions, including discrete, transient stick-slip events, which carry information about surface properties. The characteristics of these events and how the brain encodes this tactile information remain enigmatic. We found that cortical neurons show a mixture of synchronized and nontemporally correlated spikes in their tactile responses. Synchronous spikes convey the magnitude of stick-slip events by numerous aspects of temporal coding. These spikes show preferential selectivity for kinetic and kinematic whisker motion. By contrast, asynchronous spikes in each neuron convey the magnitude of stick-slip events by their discharge rates, response probability, and interspike intervals. We further show that the differentiation between these two types of activity is highly dependent on the magnitude of stick-slip events and stimulus and response history. These results suggest that cortical neurons transmit multiple components of tactile information through numerous coding strategies.

Asunto(s)

Corteza Somatosensorial , Percepción del Tacto , Animales , Corteza Somatosensorial/fisiología , Vibrisas/fisiología , Tacto/fisiología , Percepción del Tacto/fisiología , Neuronas/fisiología , Roedores

RESUMEN

The array of vibrissae on a rat's face is the first stage in a high-resolution tactile sensing system. Progressing from rostral to caudal in any vibrissae row results in an increase in whisker length and thickness. This may, in turn, provide a systematic map of separate tactile channels governed by the mechanical properties of the whiskers. To examine whether this map is expressed in a location-dependent transformation of tactile signals into whisker vibrations and neuronal responses, we monitored whiskers' movements across various surfaces and edges. We found a robust rostral-caudal (R-C) gradient of tactile information transmission in which rostral shorter vibrissae displayed a higher sensitivity and bigger differences in response to different textures, whereas longer caudal vibrissae were less sensitive. This gradient is evident in several dynamic properties of vibrissae trajectories. As rodents sample the environment with multiple vibrissae, we found that combining tactile signals from multiple vibrissae resulted in an increased sensitivity and bigger differences in response to the different textures. Nonetheless, we found that texture identity is not represented spatially across the whisker pad. Based on the responses of first-order sensory neurons, we found that they adhere to the tactile information conveyed by the vibrissae. That is, neurons innervating rostral vibrissae were better suited for texture discrimination, whereas neurons innervating caudal vibrissae were more suited for edge detection. These results suggest that the whisker array in rodents forms a sensory structure in which different facets of tactile information are transmitted through location-dependent gradient of vibrissae on the rat's face.

Asunto(s)

Percepción del Tacto/fisiología , Vibrisas/fisiología , Animales , Fenómenos Biomecánicos , Masculino , Neuronas/fisiología , Ratas Sprague-Dawley , Ganglio del Trigémino

RESUMEN

The rodent's vibrissal system is a useful model system for studying sensorimotor integration in perception. This integration determines the way in which sensory information is acquired by sensory organs and the motor commands that control them. The initial instance of sensorimotor integration in the whisker somatosensory system is implemented in the brain stem loop and may be essential to the way rodents explore and sense their environment. To examine the nature of these sensorimotor interactions, we recorded from lightly anesthetized rats in vivo and brain stem slices in vitro and isolated specific parts of this loop. We found that motor feedback to the vibrissal pad serves as a dynamic gain controller that controls the response of first-order sensory neurons by increasing and decreasing sensitivity to lower and higher tactile stimulus magnitudes, respectively. This delicate mechanism is mediated through tactile stimulus magnitude-dependent motor feedback. Conversely, tactile inputs affect the motor whisking output through influences on the rhythmic whisking circuitry, thus changing whisking kinetics. Similarly, tactile influences also modify the whisking amplitude through synaptic and intrinsic neuronal interaction in the facial nucleus, resulting in facilitation or suppression of whisking amplitude. These results point to the vast range of mechanisms underlying sensorimotor integration in the brain stem loop.NEW & NOTEWORTHY Sensorimotor integration is a process in which sensory and motor information is combined to control the flow of sensory information, as well as to adjust the motor system output. We found in the rodent's whisker somatosensory system mutual influences between tactile inputs and motor output, in which motor neurons control the flow of sensory information depending on their magnitude. Conversely, sensory information can control the magnitude and kinetics of whisker movement.

Asunto(s)

Tronco Encefálico/fisiología , Fenómenos Electrofisiológicos/fisiología , Retroalimentación Sensorial/fisiología , Actividad Motora/fisiología , Neuronas Motoras/fisiología , Percepción del Tacto/fisiología , Tacto/fisiología , Nervio Trigémino/fisiología , Vibrisas/fisiología , Animales , Electromiografía , Masculino , Técnicas de Placa-Clamp , Estimulación Física , Ratas , Ratas Sprague-Dawley

RESUMEN

The function of rodents' whisker somatosensory system is to transform tactile cues, in the form of vibrissa vibrations, into neuronal responses. It is well established that rodents can detect numerous tactile stimuli and tell them apart. However, the transformation of tactile stimuli obtained through whisker movements to neuronal responses is not well-understood. Here we examine the role of whisker velocity in tactile information transmission and its coding mechanisms. We show that in anaesthetized rats, whisker velocity is related to the radial distance of the object contacted and its own velocity. Whisker velocity is accurately and reliably coded in first-order neurons in parallel, by both the relative time interval between velocity-independent first spike latency of rapidly adapting neurons and velocity-dependent first spike latency of slowly adapting neurons. At the same time, whisker velocity is also coded, although less robustly, by the firing rates of slowly adapting neurons. Comparing first- and second-order neurons, we find similar decoding efficiencies for whisker velocity using either temporal or rate-based methods. Both coding schemes are sufficiently robust and hardly affected by neuronal noise. Our results suggest that whisker kinematic variables are coded by two parallel coding schemes and are disseminated in a similar way through various brain stem nuclei to multiple brain areas.

Asunto(s)

Potenciales Evocados Somatosensoriales , Percepción del Tacto , Vibrisas/fisiología , Adaptación Fisiológica , Animales , Fenómenos Biomecánicos , Tronco Encefálico/fisiología , Masculino , Neuronas/fisiología , Ratas , Ratas Sprague-Dawley , Tiempo de Reacción , Corteza Sensoriomotora/fisiología , Tacto , Vibrisas/inervación

RESUMEN

Texture discrimination is a fundamental function of somatosensory systems, yet the manner by which texture is coded and spatially represented in the barrel cortex are largely unknown. Using in vivo two-photon calcium imaging in the rat barrel cortex during artificial whisking against different surface coarseness or controlled passive whisker vibrations simulating different coarseness, we show that layer 2-3 neurons within barrel boundaries differentially respond to specific texture coarsenesses, while only a minority of neurons responded monotonically with increased or decreased surface coarseness. Neurons with similar preferred texture coarseness were spatially clustered. Multi-contact single unit recordings showed a vertical columnar organization of texture coarseness preference in layer 2-3. These findings indicate that layer 2-3 neurons perform high hierarchical processing of tactile information, with surface coarseness embodied by distinct neuronal subpopulations that are spatially mapped onto the barrel cortex.

Asunto(s)

Nervio Facial/fisiología , Neuronas/fisiología , Corteza Somatosensorial/fisiología , Vibrisas/fisiología , Algoritmos , Compuestos de Anilina/química , Animales , Mapeo Encefálico , Estimulación Eléctrica , Colorantes Fluorescentes/química , Microscopía Confocal , Movimiento/fisiología , Neuronas/química , Ratas Wistar , Corteza Somatosensorial/citología , Propiedades de Superficie , Xantenos/química

RESUMEN

Rodents use their whiskers to detect a variety of tactile features of their environment. They do so by using two functionally distinct whisker systems: the macrovibrissae and microvibrissae. To determine the functional role of unexplored microvibrissae, we recorded from the cortical area representing the frontobuccal pad in anesthetized rats while presenting moving textures of varying coarseness. We find that surface coarseness is coded by the discharge rates of frontobuccal pad cortical neurons. Cortical neurons can use this response measure to robustly and reliably discriminate between the different textures. While neuronal discharge rates carry tactile information, the highly reproducible firing patterns of these neurons suggest that a single spike train may contain sufficient information to encode the stimulus. Together, these results indicate that rodents may use their microvibrissae to distinguish between surfaces having subtly different textures and shapes.

Asunto(s)

Discriminación en Psicología , Corteza Somatosensorial/fisiología , Percepción del Tacto , Vibrisas/inervación , Potenciales de Acción , Animales , Masculino , Ratas , Ratas Sprague-Dawley , Tacto , Vibrisas/fisiología

RESUMEN

Rodents use their whiskers to sense their surroundings. As most of the information available to the somatosensory system originates in whiskers' primary afferents, it is essential to understand the transformation of whisker motion into neuronal activity. Here, we combined in vivo recordings in anesthetized rats with mathematical modeling to ascertain the mechanical and electrical characteristics of mechanotransduction. We found that only two synergistic processes, which reflect the dynamic interactions between (1) receptor and whisker and (2) receptor and surrounding tissue, are needed to describe mechanotransduction during passive whiskers deflection. Interactions between these processes may account for stimulus-dependent changes in the magnitude and temporal pattern of tactile responses on multiple scales. Thus, we are able to explain complex electromechanical processes underlying sensory transduction using a simple model, which captures the responses of a wide range of mechanoreceptor types to diverse sensory stimuli. This compact and precise model allows for a ubiquitous description of how mechanoreceptors encode tactile stimulus.

Asunto(s)

Mecanorreceptores/fisiología , Mecanotransducción Celular/fisiología , Corteza Somatosensorial/fisiología , Vibrisas/fisiología , Análisis de Varianza , Animales , Masculino , Modelos Neurológicos , Vías Nerviosas/fisiología , Estimulación Física , Ratas , Ratas Sprague-Dawley

RESUMEN

In their natural environment, rodents use their whiskers to locate and distinguish between objects of different textures and shapes. They do so by moving their whiskers actively as well as passively, through body and head movements. To determine the mechanisms by which surface coarseness is translated into neuronal discharges through passive whisker movements, we monitored head movements of awake behaving rats while approaching objects. We then replayed these movements in anesthetized rats, monitored the whiskers' movements across various surfaces, and concurrently recorded the activity of first-order sensory neurons. We found that whiskers, being the first stage of sensory information translation, shape transduction by amplifying small-amplitude high-frequency signals. Thus, surface coarseness is transmitted through high-velocity micromotions. Consistent with this, we find that during surface contact, discrete high-velocity movements, or stick-slip events, evoke first-order neuronal discharge. Transient ringing in whiskers, which primarily represents resonance vibrations, follows these events, but seldom causes neurons to discharge. These sensory transformations are influenced by the whiskers' biomechanical properties. To determine the resemblance of these tactile transformations during passive whisker movements and active whisking, we induced artificial whisking across various surface textures. We found that the processes by which tactile information becomes available to the animal are similar for these different modes of behavior. Together, these findings indicate that the temporal bandpass properties for spike generation in first-order neurons are matched by the biomechanical characteristics of whiskers, which translate surface coarseness into high-frequency whisker micromotions. These properties enable rodents to acquire tactile information through passive and active movements of their whiskers.

Asunto(s)

Percepción del Tacto/fisiología , Tacto/fisiología , Vibración , Vibrisas/inervación , Potenciales de Acción/fisiología , Vías Aferentes/fisiología , Animales , Biofisica , Análisis de Fourier , Movimientos de la Cabeza , Masculino , Estimulación Física/métodos , Ratas , Ratas Sprague-Dawley , Células Receptoras Sensoriales/fisiología , Umbral Sensorial/fisiología , Estadística como Asunto , Ganglio del Trigémino/citología , Vigilia

RESUMEN

What patterns of synaptic input cause cortical neurons to fire action potentials? Are they stochastic in nature, or do action potentials arise from the specific timing of synaptic input? We addressed these questions by measuring the membrane potential fluctuations associated with the generation of visually evoked action potentials in cat striate cortical neurons in vivo. In response to visual stimulation, action potentials occurred at the crest of large-amplitude, transient depolarizations (TDs) riding on sustained depolarization of the membrane potential. The magnitude, duration and rate of depolarization of these transient events were tuned for stimulus orientation. Using numerical simulations, we find that these transient events can arise from the temporal interplay between synchronous excitation and inhibition. To validate these findings, we made conductance measurements, at the preferred stimulus orientation, and showed that the TDs arise either from an increase in excitatory conductance, or from a combination of increased excitatory and decreased inhibitory conductance, both riding on sustained changes in synaptic conductances. The properties of the TDs and their underlying conductance suggest that they arise from a specific temporal interplay between synchronous excitatory and inhibitory synaptic inputs. Our results illustrate a mechanism by which the timing of synaptic inputs determines much of the spiking activity in striate cortical neurons.

Asunto(s)

Potenciales de Acción/fisiología , Sincronización Cortical , Neuronas/fisiología , Transmisión Sináptica/fisiología , Corteza Visual/fisiología , Percepción Visual/fisiología , Animales , Gatos , Membrana Celular/fisiología , Interpretación Estadística de Datos , Electrofisiología , Potenciales Postsinápticos Excitadores/fisiología , Femenino , Potenciales Postsinápticos Inhibidores/fisiología , Masculino , Potenciales de la Membrana/fisiología , Inhibición Neural/fisiología , Orientación/fisiología , Reconocimiento Visual de Modelos/fisiología , Estimulación Luminosa , Tiempo de Reacción/fisiología , Factores de Tiempo

RESUMEN

Rodents in their natural environment use their whiskers to distinguish between surfaces having subtly different textures and shapes. They do so by actively sweeping their whiskers across surfaces in a rhythmic motion. To determine how textures are transformed into vibration signals in whiskers and how these vibrations are expressed in neuronal discharges, we induced active whisking in anesthetized rats, monitored the movement of whiskers across surfaces, and concurrently recorded from trigeminal ganglion (TG) neurons. We show that tactile information is transmitted through high-frequency micromotions superimposed on whisking macro motions. Consistent with this, we find that in most TG neurons, spike activity, and high-frequency micromotions are closely correlated. To determine whether these vibration signals can support texture discrimination, we examined their dependence on surface roughness and found that both vibration signals carry information about surface coarseness. Despite a large variability in this translation process, different textures are translated into distinct vibrations profiles. These profiles depend on whiskers properties, on radial distance to the surface, and on whisking frequency. Using the characteristics of these signals, we employ linear discriminant analysis and found that all whiskers were able to discriminate between different textures. While deteriorating with radial distance, this classification did not depend on whisking frequency. Finally, increasing the number of whisks and integrating tactile information from multiple whiskers improved texture discrimination. These results indicate that surface roughness is translated into distinct whisker vibration signals that result in neuronal discharges. However, due to the dynamic nature of this translation process, we propose that texture discrimination may require the integration of signals from multiple spatial and temporal sensory channels to disambiguate surface roughness.

Asunto(s)

Dinámicas no Lineales , Percepción del Tacto/fisiología , Vibración , Vibrisas/fisiología , Potenciales de Acción/fisiología , Animales , Relación Dosis-Respuesta en la Radiación , Estimulación Eléctrica/métodos , Masculino , Neuronas/fisiología , Estimulación Física/métodos , Ratas , Ratas Sprague-Dawley , Tiempo de Reacción , Ganglio del Trigémino/citología

RESUMEN

An essential component of feedback and top-down information in the cortical column arrives at layer 1 (L1) where it contacts distal dendrites of pyramidal neurons. Although much is known about the anatomical organization of L1 fibers, their contribution to sensory information processing remains to be determined. We assessed the physiological significance of L1 inputs by performing extracellular recordings in vivo from neurons in the primary somatosensory cortex of rodents. We found that blocking activity in L1 increases whisker-evoked response magnitude and variance, suggesting that L1 exerts an inhibitory influence on whisker responses. However, when pairing L1 stimulation with whisker deflection, the interval between the stimuli determined the outcome of the interaction, with facilitation of sensory responses dominating the short intervals (10 ms). These temporal interactions resulted in a time-dependent regulation of direction tuning of cortical neurons. The synaptic mechanisms underlying L1 inputs' influences were examined using whole cell recordings in vitro while pairing L1 and white-matter stimulations. We found time-dependent, layer-specific differences in synaptic summation of the two inputs, with supralinearity at shorter intervals and sublinearity at longer intervals that resulted mainly from shunting inhibition. Taken together, our results demonstrate that L1 inputs impose a time- and layer-specific regulation on sensory-evoked responses. This in turn may lead to a dynamic transmission of sensory information in the somatosensory cortex.

Asunto(s)

Neocórtex/fisiología , Sensación/fisiología , Algoritmos , Anestésicos Locales/farmacología , Animales , Interpretación Estadística de Datos , Estimulación Eléctrica , Potenciales Evocados/efectos de los fármacos , Potenciales Evocados/fisiología , Antagonistas de Aminoácidos Excitadores/farmacología , Espacio Extracelular/efectos de los fármacos , Espacio Extracelular/fisiología , Masculino , Ratones , Microelectrodos , Neocórtex/citología , Vías Nerviosas/citología , Vías Nerviosas/efectos de los fármacos , Vías Nerviosas/fisiología , Dinámicas no Lineales , Técnicas de Placa-Clamp , Estimulación Física , Quinoxalinas/farmacología , Sensación/efectos de los fármacos , Sinapsis/efectos de los fármacos , Sinapsis/fisiología , Transmisión Sináptica/efectos de los fármacos , Transmisión Sináptica/fisiología , Tetrodotoxina/farmacología , Factores de Tiempo , Vibrisas/inervación , Vibrisas/fisiología

RESUMEN

Gain modulation is a ubiquitous phenomenon in cortical neurons, providing flexibility to operate under changing conditions. The prevailing view is that this modulation reflects a change in the relationship between mean input and output firing rate brought about by variation in neuronal membrane characteristics. An alternative mechanism is proposed for neuronal gain modulation that takes into account the capability of cortical neurons to process spatiotemporal synaptic correlations. Through the use of numerical simulations, it is shown that voltage-gated and leak conductances, membrane potential, noise, and input firing rate modify the sensitivity of cortical neurons to the degree of temporal correlation between their synaptic inputs. These changes are expressed in a change of the temporal window for synaptic integration and the range of input correlation over which response probability is graded. The study also demonstrates that temporal integration depends on the distance between the inputs and that this interplay of space and time is modulated by voltage-gated and leak conductances. Thus, gain modulation may reflect a change in the relationship between spatiotemporal synaptic correlations and output firing probability. It is further proposed that by acting synergistically with the network, dynamic spatiotemporal synaptic integration in cortical neurons may serve a functional role in the formation of dynamic cell assemblies.

Asunto(s)

Corteza Cerebral/citología , Modelos Neurológicos , Neuronas/fisiología , Dinámicas no Lineales , Sinapsis/fisiología , Transmisión Sináptica/fisiología , Animales , Conductividad Eléctrica , Activación del Canal Iónico/fisiología , Potenciales de la Membrana/fisiología , Inhibición Neural/fisiología , Técnicas de Placa-Clamp/métodos , Probabilidad , Factores de Tiempo

RESUMEN

To facilitate the characterization of cortical neuronal function, the responses of cells in cat area 17 to intracellular injection of current pulses were quantitatively analyzed. A variety of response variables were used to separate the cells into subtypes using cluster analysis. Four main classes of neurons could be clearly distinguished: regular spiking (RS), fast spiking (FS), intrinsic bursting (IB), and chattering (CH). Each of these contained significant subclasses. RS neurons were characterized by trains of action potentials that exhibited spike frequency adaptation. Morphologically, these cells were spiny stellate cells in layer 4 and pyramidal cells in layers 2, 3, 5, and 6. FS neurons had short-duration action potentials (<0.5 ms at half height), little or no spike frequency adaptation, and a steep relationship between injected current intensity and spike discharge frequency. Morphologically, these cells were sparsely spiny or aspiny nonpyramidal cells. IB neurons typically generated a low frequency (<425 Hz) burst of spikes at the beginning of a depolarizing current pulse followed by a tonic train of action potentials for the remainder of the pulse. These cells were observed in all cortical layers, but were most abundant in layer 5. Finally, CH neurons generated repetitive, high-frequency (350-700 Hz) bursts of short-duration (<0.55 ms) action potentials. Morphologically, these cells were layer 2-4 (mainly layer 3) pyramidal or spiny stellate neurons. These results indicate that firing properties do not form a continuum and that cortical neurons are members of distinct electrophysiological classes and subclasses.

Asunto(s)

Potenciales de Acción/fisiología , Células Piramidales/fisiología , Corteza Visual/citología , Corteza Visual/fisiología , Adaptación Fisiológica/fisiología , Animales , Gatos , Tamaño de la Célula/fisiología , Análisis por Conglomerados , Impedancia Eléctrica , Estimulación Eléctrica , Electrofisiología , Femenino , Masculino , Periodicidad , Células Piramidales/citología , Campos Visuales/fisiología

RESUMEN

Several theories have proposed a functional role for response synchronization in sensory perception. Critics of these theories have argued that selective synchronization is physiologically implausible when cortical networks operate at high levels of activity. Using intracellular recordings from visual cortex in vivo, in combination with numerical simulations, we find dynamic changes in spike threshold that reduce cellular sensitivity to slow depolarizations and concurrently increase the relative sensitivity to rapid depolarizations. Consistent with this, we find that spike activity and high-frequency fluctuations in membrane potential are closely correlated and that both are more tightly tuned for stimulus orientation than the mean membrane potential. These findings suggest that under high-input conditions the spike-generating mechanism adaptively enhances the sensitivity to synchronous inputs while simultaneously decreasing the sensitivity to temporally uncorrelated inputs.

Asunto(s)

Adaptación Ocular/fisiología , Neuronas/fisiología , Corteza Visual/citología , Corteza Visual/fisiología , Potenciales de Acción/fisiología , Animales , Gatos , Potenciales Evocados Visuales/fisiología , Femenino , Masculino , Orientación/fisiología , Umbral Sensorial/fisiología