-
The Journal of Neuroscience : the... Jun 2021Rapid sensory adaptation is observed across all sensory systems, and strongly shapes sensory percepts in complex sensory environments. Yet despite its ubiquity and...
Rapid sensory adaptation is observed across all sensory systems, and strongly shapes sensory percepts in complex sensory environments. Yet despite its ubiquity and likely necessity for survival, the mechanistic basis is poorly understood. A wide range of primarily and anesthetized studies have demonstrated the emergence of adaptation at the level of primary sensory cortex, with only modest signatures in earlier stages of processing. The nature of rapid adaptation and how it shapes sensory representations during wakefulness, and thus the potential role in perceptual adaptation, is underexplored, as are the mechanisms that underlie this phenomenon. To address these knowledge gaps, we recorded spiking activity in primary somatosensory cortex (S1) and the upstream ventral posteromedial (VPm) thalamic nucleus in the vibrissa pathway of awake male and female mice, and quantified responses to whisker stimuli delivered in isolation and embedded in an adapting sensory background. We found that cortical sensory responses were indeed adapted by persistent sensory stimulation; putative excitatory neurons were profoundly adapted, and inhibitory neurons only modestly so. Further optogenetic manipulation experiments and network modeling suggest this largely reflects adaptive changes in synchronous thalamic firing combined with robust engagement of feedforward inhibition, with little contribution from synaptic depression. Taken together, these results suggest that cortical adaptation in the regime explored here results from changes in the timing of thalamic input, and the way in which this differentially impacts cortical excitation and feedforward inhibition, pointing to a prominent role of thalamic gating in rapid adaptation of primary sensory cortex. Rapid adaptation of sensory activity strongly shapes representations of sensory inputs across all sensory pathways over the timescale of seconds, and has profound effects on sensory perception. Despite its ubiquity and theoretical role in the efficient encoding of complex sensory environments, the mechanistic basis is poorly understood, particularly during wakefulness. In this study in the vibrissa pathway of awake mice, we show that cortical representations of sensory inputs are strongly shaped by rapid adaptation, and that this is mediated primarily by adaptive gating of the thalamic inputs to primary sensory cortex and the differential way in which these inputs engage cortical subpopulations of neurons.
Topics: Adaptation, Physiological; Animals; Female; Male; Mice; Somatosensory Cortex; Thalamus; Vibrissae; Wakefulness
PubMed: 33986072
DOI: 10.1523/JNEUROSCI.3018-20.2021 -
PLoS Computational Biology May 2021Extracellular recording is an accessible technique used in animals and humans to study the brain physiology and pathology. As the number of recording channels and their...
Extracellular recording is an accessible technique used in animals and humans to study the brain physiology and pathology. As the number of recording channels and their density grows it is natural to ask how much improvement the additional channels bring in and how we can optimally use the new capabilities for monitoring the brain. Here we show that for any given distribution of electrodes we can establish exactly what information about current sources in the brain can be recovered and what information is strictly unobservable. We demonstrate this in the general setting of previously proposed kernel Current Source Density method and illustrate it with simplified examples as well as using evoked potentials from the barrel cortex obtained with a Neuropixels probe and with compatible model data. We show that with conceptual separation of the estimation space from experimental setup one can recover sources not accessible to standard methods.
Topics: Animals; Brain; Computational Biology; Computer Simulation; Electrodes; Evoked Potentials; Extracellular Space; Humans; Male; Models, Neurological; Rats; Rats, Wistar; Somatosensory Cortex; Vibrissae
PubMed: 33989280
DOI: 10.1371/journal.pcbi.1008615 -
Anatomical Record (Hoboken, N.J. : 2007) Mar 2022Pinniped vibrissae are well-adapted to sensing in an aquatic environment, by being morphologically diverse and more sensitive than those of terrestrial species. However,...
Pinniped vibrissae are well-adapted to sensing in an aquatic environment, by being morphologically diverse and more sensitive than those of terrestrial species. However, it is both challenging and time-consuming to measure vibrissal sensitivity in many species. In terrestrial species, the infraorbital foramen (IOF) area is associated with vibrissal sensitivity and increases with vibrissal number. While pinnipeds are thought to have large IOF areas, this has not yet been systematically measured before. We investigated vibrissal morphology, IOF area, and skull size in 16 species of pinniped and 12 terrestrial Carnivora species. Pinnipeds had significantly larger skulls and IOF areas, longer vibrissae, and fewer vibrissae than the other Carnivora species. IOF area and vibrissal number were correlated in Pinnipeds, just as they are in terrestrial mammals. However, despite pinnipeds having significantly fewer vibrissae than other Carnivora species, their IOF area was not smaller, which might be due to pinnipeds having vibrissae that are innervated more. We propose that investigating normalized IOF area per vibrissa will offer an alternative way to approximate gross individual vibrissal sensitivity in pinnipeds and other mammalian species. Our data show that many species of pinniped, and some species of felids, are likely to have strongly innervated individual vibrissae, since they have high values of normalized IOF area per vibrissa. We suggest that species that hunt moving prey items in the dark will have more sensitive and specialized vibrissae, especially as they have to integrate between individual vibrissal signals to calculate the direction of moving prey during hunting.
Topics: Animals; Caniformia; Carnivora; Vibrissae
PubMed: 34076956
DOI: 10.1002/ar.24683 -
Current Biology : CB Aug 2020Does sensory input flow into the brain as a stream, or does it come in waves? New research shows that tactile information in the cortex rises and falls in phase with the...
Does sensory input flow into the brain as a stream, or does it come in waves? New research shows that tactile information in the cortex rises and falls in phase with the forward and back motion of whiskers during surface exploration.
Topics: Animals; Brain; Touch; Touch Perception; Vibrissae
PubMed: 32810452
DOI: 10.1016/j.cub.2020.06.087 -
Journal of Affective Disorders Mar 2022Stroke is a life-changing event as stroke survivors experience changes in personality, emotions and mood. We investigated the effect of xenon gas encapsulated in...
Stroke is a life-changing event as stroke survivors experience changes in personality, emotions and mood. We investigated the effect of xenon gas encapsulated in liposomes on stroke-generated sensorimotor impairments, and anxiety- and depression-like phenotypes. Ischemic stroke was created by the intraluminal middle cerebral artery occlusion (MCAO) for 6 h followed by reperfusion in rats. Xenon-liposome (6 mg/kg, intravenous) treatment was given multiple times starting at 2 h post-ischemia through 6 h (5X), and once-daily for next 3 days. Rats underwent ischemic injury displayed sensorimotor deficits in the adhesive removal, vibrissae-evoked forelimb placement and rotarod tests. These animals also made lesser entries and spent less time on open arms of the elevated-plus maze and swam more in passive mode in the forced swimming test, indicating anxiety- and depression-like behaviors at 28- and 35-days post-injury, respectively. Repeated intravenous treatment with xenon-liposomes ameliorated these behavioral aberrations (p < 0.05). Gut microbiome analysis (16S ribosomal-RNA gene sequencing) showed a decrease in the Clostridium clusters XI, XIVa, XVIII and Lactobacillus bacterium, and increase of the Prevotella in the xenon-liposome group. No microbiota communities were majorly affected across the treatments. Moreover, xenon treatment group showed augmented plasma levels of IL-6 cytokines (∼5 fold) on day-35 post-ischemia, while no change was noticed in the IL-1β, IL-4, IL-10, IL-13 and MCP-1 levels. Our data highlights the safety, behavioral recovery and reversal of post-stroke brain injury following xenon-liposome treatment in an extended ischemic model. These results show the potential for this treatment strategy to be translated to patients with stroke.
Topics: Animals; Anxiety; Brain Injuries; Cytokines; Disease Models, Animal; Humans; Infarction, Middle Cerebral Artery; Rats; Xenon
PubMed: 34990636
DOI: 10.1016/j.jad.2022.01.025 -
Frontiers in Microbiology 2023Herpes simplex virus 1 (HSV-1) is a widely distributed virus. HSV-1 is a growing public health concern due to the emergence of drug-resistant strains and the current...
Herpes simplex virus 1 (HSV-1) is a widely distributed virus. HSV-1 is a growing public health concern due to the emergence of drug-resistant strains and the current lack of a clinically specific drug for treatment. In recent years, increasing attention has been paid to the development of peptide antivirals. Natural host-defense peptides which have uniquely evolved to protect the host have been reported to have antiviral properties. Cathelicidins are a family of multi-functional antimicrobial peptides found in almost all vertebrate species and play a vital role in the immune system. In this study, we demonstrated the anti-HSV-1 effect of an antiviral peptide named WL-1 derived from human cathelicidin. We found that WL-1 inhibited HSV-1 infection in epithelial and neuronal cells. Furthermore, the administration of WL-1 improved the survival rate and reduced viral load and inflammation during HSV-1 infection via ocular scarification. Moreover, facial nerve dysfunction, involving the abnormal blink reflex, nose position, and vibrissae movement, and pathological injury were prevented when HSV-1 ear inoculation-infected mice were treated with WL-1. Together, our findings demonstrate that WL-1 may be a potential novel antiviral agent against HSV-1 infection-induced facial palsy.
PubMed: 37342565
DOI: 10.3389/fmicb.2023.1201505 -
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 -
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