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PLoS Biology Oct 2020The 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...
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.
Topics: Animals; Biomechanical Phenomena; Male; Neurons; Rats, Sprague-Dawley; Touch Perception; Trigeminal Ganglion; Vibrissae
PubMed: 33090990
DOI: 10.1371/journal.pbio.3000699 -
Scientific Reports Aug 2021The eyelid motor system has been used for years as an experimental model for studying the neuronal mechanisms underlying motor and cognitive learning, mainly with...
The eyelid motor system has been used for years as an experimental model for studying the neuronal mechanisms underlying motor and cognitive learning, mainly with classical conditioning procedures. Nonetheless, it is not known yet which brain structures, or neuronal mechanisms, are responsible for the acquisition, storage, and expression of these motor responses. Here, we studied the temporal correlation between unitary activities of identified eyelid and vibrissae motor cortex neurons and the electromyographic activity of the orbicularis oculi and vibrissae muscles and magnetically recorded eyelid positions during classical conditioning of eyelid and vibrissae responses, using both delay and trace conditioning paradigms in behaving mice. We also studied the involvement of motor cortex neurons in reflexively evoked eyelid responses and the kinematics and oscillatory properties of eyelid movements evoked by motor cortex microstimulation. Results show the involvement of the motor cortex in the performance of conditioned responses elicited during the classical conditioning task. However, a timing correlation analysis showed that both electromyographic activities preceded the firing of motor cortex neurons, which must therefore be related more with the reinforcement and/or proper performance of the conditioned responses than with their acquisition and storage.
Topics: Animals; Conditioning, Classical; Eyelids; Male; Mice, Inbred C57BL; Motor Cortex; Motor Neurons; Vibrissae; Mice
PubMed: 34404871
DOI: 10.1038/s41598-021-96153-6 -
Proceedings of the National Academy of... Dec 2020Seasonal cycles govern life on earth, from setting the time for the mating season to influencing migrations and governing physiological conditions like hibernation. The...
Seasonal cycles govern life on earth, from setting the time for the mating season to influencing migrations and governing physiological conditions like hibernation. The effect of such changing conditions on behavior is well-appreciated, but their impact on the brain remains virtually unknown. We investigate long-term seasonal changes in the mammalian brain, known as Dehnel's effect, where animals exhibit plasticity in body and brain sizes to counter metabolic demands in winter. We find large seasonal variation in cellular architecture and neuronal activity in the smallest terrestrial mammal, the Etruscan shrew, Their brain, and specifically their neocortex, shrinks in winter. Shrews are tactile hunters, and information from whiskers first reaches the somatosensory cortex layer 4, which exhibits a reduced width (-28%) in winter. Layer 4 width (+29%) and neuron number (+42%) increase the following summer. Activity patterns in the somatosensory cortex show a prominent reduction of touch-suppressed neurons in layer 4 (-55%), the most metabolically active layer. Loss of inhibitory gating occurs with a reduction in parvalbumin-positive interneurons, one of the most active neuronal subtypes and the main regulators of inhibition in layer 4. Thus, a reduction in neurons in layer 4 and particularly parvalbumin-positive interneurons may incur direct metabolic benefits. However, changes in cortical balance can also affect the threshold for detecting sensory stimuli and impact prey choice, as observed in wild shrews. Thus, seasonal neural adaptation can offer synergistic metabolic and behavioral benefits to the organism and offer insights on how neural systems show adaptive plasticity in response to ecological demands.
Topics: Animals; Energy Metabolism; Female; Hibernation; Magnetic Resonance Imaging; Male; Neuronal Plasticity; Neurons; Organ Size; Seasons; Shrews; Somatosensory Cortex; Touch Perception; Vibrissae
PubMed: 33257560
DOI: 10.1073/pnas.1922888117 -
Current Biology : CB May 2023Cortical activity patterns occupy a small subset of possible network states. If this is due to intrinsic network properties, microstimulation of sensory cortex should...
Cortical activity patterns occupy a small subset of possible network states. If this is due to intrinsic network properties, microstimulation of sensory cortex should evoke activity patterns resembling those observed during natural sensory input. Here, we use optical microstimulation of virally transfected layer 2/3 pyramidal neurons in the mouse primary vibrissal somatosensory cortex to compare artificially evoked activity with natural activity evoked by whisker touch and movement ("whisking"). We find that photostimulation engages touch- but not whisking-responsive neurons more than expected by chance. Neurons that respond to photostimulation and touch or to touch alone exhibit higher spontaneous pairwise correlations than purely photoresponsive neurons. Exposure to several days of simultaneous touch and optogenetic stimulation raises both overlap and spontaneous activity correlations among touch and photoresponsive neurons. We thus find that cortical microstimulation engages existing cortical representations and that repeated co-presentation of natural and artificial stimulation enhances this effect.
Topics: Mice; Animals; Somatosensory Cortex; Parietal Lobe; Movement; Touch; Touch Perception; Vibrissae
PubMed: 37130521
DOI: 10.1016/j.cub.2023.03.085 -
Cell Reports Dec 2023Sensory cortical areas are organized into topographic maps representing the sensory epithelium. Interareal projections typically connect topographically matched...
Sensory cortical areas are organized into topographic maps representing the sensory epithelium. Interareal projections typically connect topographically matched subregions across areas. Because matched subregions process the same stimulus, their interaction is central to many computations. Here, we ask how topographically matched subregions of primary and secondary vibrissal somatosensory cortices (vS1 and vS2) interact during active touch. Volumetric calcium imaging in mice palpating an object with two whiskers revealed a sparse population of highly responsive, broadly tuned touch neurons especially pronounced in layer 2 of both areas. These rare neurons exhibited elevated synchrony and carried most touch-evoked activity in both directions. Lesioning the subregion of either area responding to the spared whiskers degraded touch responses in the unlesioned area, with whisker-specific vS1 lesions degrading whisker-specific vS2 touch responses. Thus, a sparse population of broadly tuned touch neurons dominates vS1-vS2 communication in both directions, and topographically matched vS1 and vS2 subregions recurrently amplify whisker touch activity.
Topics: Mice; Animals; Touch; Touch Perception; Neurons; Somatosensory Cortex; Vibrissae; Physical Stimulation
PubMed: 38064338
DOI: 10.1016/j.celrep.2023.113532 -
PLoS Computational Biology Jan 2021The connection between stimulus perception and time perception remains unknown. The present study combines human and rat psychophysics with sensory cortical neuronal...
The connection between stimulus perception and time perception remains unknown. The present study combines human and rat psychophysics with sensory cortical neuronal firing to construct a computational model for the percept of elapsed time embedded within sense of touch. When subjects judged the duration of a vibration applied to the fingertip (human) or whiskers (rat), increasing stimulus intensity led to increasing perceived duration. Symmetrically, increasing vibration duration led to increasing perceived intensity. We modeled real spike trains recorded from vibrissal somatosensory cortex as input to dual leaky integrators-an intensity integrator with short time constant and a duration integrator with long time constant-generating neurometric functions that replicated the actual psychophysical functions of rats. Returning to human psychophysics, we then confirmed specific predictions of the dual leaky integrator model. This study offers a framework, based on sensory coding and subsequent accumulation of sensory drive, to account for how a feeling of the passage of time accompanies the tactile sensory experience.
Topics: Action Potentials; Adult; Animals; Computational Biology; Humans; Male; Models, Neurological; Psychophysics; Rats; Rats, Wistar; Somatosensory Cortex; Task Performance and Analysis; Time Perception; Vibration; Vibrissae; Young Adult
PubMed: 33513135
DOI: 10.1371/journal.pcbi.1008668 -
ELife Oct 2019The active properties of dendrites can support local nonlinear operations, but previous imaging and electrophysiological measurements have produced conflicting views...
The active properties of dendrites can support local nonlinear operations, but previous imaging and electrophysiological measurements have produced conflicting views regarding the prevalence and selectivity of local nonlinearities in vivo. We imaged calcium signals in pyramidal cell dendrites in the motor cortex of mice performing a tactile decision task. A custom microscope allowed us to image the soma and up to 300 μm of contiguous dendrite at 15 Hz, while resolving individual spines. New analysis methods were used to estimate the frequency and spatial scales of activity in dendritic branches and spines. The majority of dendritic calcium transients were coincident with global events. However, task-associated calcium signals in dendrites and spines were compartmentalized by dendritic branching and clustered within branches over approximately 10 μm. Diverse behavior-related signals were intermingled and distributed throughout the dendritic arbor, potentially supporting a large learning capacity in individual neurons.
Topics: Animals; Calcium Signaling; Decision Making; Mice; Microscopy; Motor Cortex; Nerve Net; Pyramidal Cells; Touch Perception; Vibrissae
PubMed: 31663507
DOI: 10.7554/eLife.46966 -
Neuron May 2020Cortical sensory areas are supposed to encode immediate sensory inputs. In this issue of Neuron, Condylis et al. (2020) show that they can also recall information about...
Cortical sensory areas are supposed to encode immediate sensory inputs. In this issue of Neuron, Condylis et al. (2020) show that they can also recall information about a past event when in need of comparing two temporally segregated sensory inputs.
Topics: Animals; Neurons; Sensation; Somatosensory Cortex; Vibrissae
PubMed: 32380049
DOI: 10.1016/j.neuron.2020.04.014 -
Scientific Reports Jun 2021Neuronal activities underlying a percept are constrained by the physics of sensory signals. In the tactile sense such constraints are frictional stick-slip events,...
Neuronal activities underlying a percept are constrained by the physics of sensory signals. In the tactile sense such constraints are frictional stick-slip events, occurring, amongst other vibrotactile features, when tactile sensors are in contact with objects. We reveal new biomechanical phenomena about the transmission of these microNewton forces at the tip of a rat's whisker, where they occur, to the base where they engage primary afferents. Using high resolution videography and accurate measurement of axial and normal forces at the follicle, we show that the conical and curved rat whisker acts as a sign-converting amplification filter for moment to robustly engage primary afferents. Furthermore, we present a model based on geometrically nonlinear Cosserat rod theory and a friction model that recreates the observed whole-beam whisker dynamics. The model quantifies the relation between kinematics (positions and velocities) and dynamic variables (forces and moments). Thus, only videographic assessment of acceleration is required to estimate forces and moments measured by the primary afferents. Our study highlights how sensory systems deal with complex physical constraints of perceptual targets and sensors.
Topics: Animals; Male; Rats; Rats, Sprague-Dawley; Touch; Touch Perception; Vibrissae
PubMed: 34193889
DOI: 10.1038/s41598-021-92770-3 -
PLoS Biology May 2020Animals 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... (Comparative Study)
Comparative Study
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.
Topics: Adaptation, Physiological; Animals; Biomechanical Phenomena; Exploratory Behavior; Feedback, Sensory; Head Movements; Locomotion; Male; Rats, Wistar; Vibrissae
PubMed: 32453721
DOI: 10.1371/journal.pbio.3000571