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ELife Apr 2021Premotor circuits in the brainstem project to pools of orofacial motoneurons to execute essential motor action such as licking, chewing, breathing, and in rodent,...
Premotor circuits in the brainstem project to pools of orofacial motoneurons to execute essential motor action such as licking, chewing, breathing, and in rodent, whisking. Previous transsynaptic tracing studies only mapped orofacial premotor circuits in neonatal mice, but the adult circuits remain unknown as a consequence of technical difficulties. Here, we developed a three-step monosynaptic transsynaptic tracing strategy to identify premotor neurons controlling vibrissa, tongue protrusion, and jaw-closing muscles in the adult mouse. We registered these different groups of premotor neurons onto the Allen mouse brain common coordinate framework (CCF) and consequently generated a combined 3D orofacial premotor atlas, revealing unique spatial organizations of distinct premotor circuits. We further uncovered premotor neurons that simultaneously innervate multiple motor nuclei and, consequently, are likely to coordinate different muscles involved in the same orofacial motor actions. Our method for tracing adult premotor circuits and registering to Allen CCF is generally applicable and should facilitate the investigations of motor controls of diverse behaviors.
Topics: Animals; Atlases as Topic; Female; Jaw; Male; Masseter Muscle; Mice; Mice, Inbred C57BL; Motor Cortex; Motor Neurons; Mouth; Tongue; Vibrissae
PubMed: 33904410
DOI: 10.7554/eLife.67291 -
Acta Neurobiologiae Experimentalis 1998A change in vibrissae complement in rodents leads to long-term changes in vibrissae dominance. These changes involve both potentiation of spared vibrissae responses and... (Review)
Review
A change in vibrissae complement in rodents leads to long-term changes in vibrissae dominance. These changes involve both potentiation of spared vibrissae responses and suppression of deprived vibrissae responses in adolescent animals. In adult animals only potentiation of spared vibrissae responses was detected. Suppression exhibits hetero- and homosynaptic components and appears to be cortical in origin, as is potentiation. The time course for potentiation and suppression in the barrel cortex of adolescent rats is different, with suppression preceeding potentiation by at least one week. There seems to be no critical period for potentiation in superficial layers of barrel cortex, but there is a critical period for suppression. Suppression cannot be evoked if plasticity is induced later than at 6 months of age nor maintained if experimental manipulations begin later than at three months. The molecular mechanisms that underlie plastic changes in the barrel cortex still remain unclear, although alpha-CamKII and to lesser extend alpha/beta-CREB appear to be involved.
Topics: Animals; Motor Cortex; Rats; Rodentia; Vibrissae
PubMed: 9949558
DOI: 10.55782/ane-1998-1287 -
Proceedings of the National Academy of... Jul 2021As it becomes possible to simulate increasingly complex neural networks, it becomes correspondingly important to model the sensory information that animals actively...
As it becomes possible to simulate increasingly complex neural networks, it becomes correspondingly important to model the sensory information that animals actively acquire: the biomechanics of sensory acquisition directly determines the sensory input and therefore neural processing. Here, we exploit the tractable mechanics of the well-studied rodent vibrissal ("whisker") system to present a model that can simulate the signals acquired by a full sensor array actively sampling the environment. Rodents actively "whisk" ∼60 vibrissae (whiskers) to obtain tactile information, and this system is therefore ideal to study closed-loop sensorimotor processing. The simulation framework presented here, , incorporates realistic morphology of the rat whisker array to predict the time-varying mechanical signals generated at each whisker base during sensory acquisition. Single-whisker dynamics were optimized based on experimental data and then validated against free tip oscillations and dynamic responses to collisions. The model is then extrapolated to include all whiskers in the array, incorporating each whisker's individual geometry. Simulation examples in laboratory and natural environments demonstrate that can predict input signals during various behaviors, currently impossible in the biological animal. In one exemplary use of the model, the results suggest that active whisking increases in-plane whisker bending compared to passive stimulation and that principal component analysis can reveal the relative contributions of whisker identity and mechanics at each whisker base to the vibrissotactile response. These results highlight how interactions between array morphology and individual whisker geometry and dynamics shape the signals that the brain must process.
Topics: Animals; Behavior, Animal; Models, Neurological; Physical Stimulation; Rats; Signal Transduction; Time Factors; Touch; Vibrissae
PubMed: 34210794
DOI: 10.1073/pnas.2011905118 -
Current Biology : CB Mar 2017The delineation of sensorimotor circuits that guide exploration begins with an understanding of the pattern of motor outputs [1]. These motor patterns provide a clue to...
The delineation of sensorimotor circuits that guide exploration begins with an understanding of the pattern of motor outputs [1]. These motor patterns provide a clue to the form of the underlying circuits [2-4] (but see [5]). We focus on the behaviors that rodents use to explore their peripersonal space through goal-directed positioning of their nose, head, and vibrissae. Rodents sniff in response to novel odors, reward expectation, and as part of social interactions [6-12]. Sniffing serves olfaction [13, 14], while whisking synchronized to sniffing serves vibrissa-based touch [6, 15, 16]. We quantify the ethology of exploratory nose and head movements in relation to breathing. We find that sniffing is accompanied by prominent lateral and vertical deflections of the nose, i.e., twitches, which are driven by activation of the deflector nasi muscles [17]. On the timescale of individual breaths, nose motion is rhythmic and has a maximum deflection following the onset of inspiration. On a longer timescale, excursions of the nose persist for several breaths and are accompanied by an asymmetry in vibrissa positioning toward the same side of the face. Such directed deflections can be triggered by a lateralized source of odor. Lastly, bobbing of the head as the animal cranes and explores is phase-locked to sniffing and to movement of the nose. These data, along with prior results on the resetting of the whisk cycle at the onset of inspiration [15, 16, 18], reveal that the onset of each breath initiates a "snapshot" of the orofacial sensory environment. VIDEO ABSTRACT.
Topics: Animals; Exploratory Behavior; Female; Head Movements; Motor Activity; Nose; Rats; Rats, Long-Evans; Respiration; Smell; Touch; Vibrissae
PubMed: 28216320
DOI: 10.1016/j.cub.2017.01.013 -
The Journal of Neuroscience : the... Jul 2017The whisker system is an important sensory organ with extensive neural representations in the brain of the mouse. Patterned neural modules (barrelettes) in the...
The whisker system is an important sensory organ with extensive neural representations in the brain of the mouse. Patterned neural modules (barrelettes) in the ipsilateral principal sensory nucleus of the trigeminal nerve (PrV) correspond to the whiskers. Axons of the PrV barrelette neurons cross the midline and confer the whisker-related patterning to the contralateral ventroposteromedial nucleus of the thalamus, and subsequently to the cortex. In this way, specific neural modules called barreloids and barrels in the contralateral thalamus and cortex represent each whisker. Partial midline crossing of the PrV axons, in a conditional Robo3 mutant () mouse line, leads to the formation of bilateral whisker maps in the ventroposteromedial, as well as the barrel cortex. We used voltage-sensitive dye optical imaging and somatosensory and motor behavioral tests to characterize the consequences of bifacial maps in the thalamocortical system. Voltage-sensitive dye optical imaging verified functional, bilateral whisker representation in the barrel cortex and activation of distinct cortical loci following ipsilateral and contralateral stimulation of the specific whiskers. The mutant animals were comparable with the control animals in sensorimotor tests. However, they showed noticeable deficits in all of the whisker-dependent or -related tests, including Y-maze exploration, horizontal surface approach, bridge crossing, gap crossing, texture discrimination, floating in water, and whisking laterality. Our results indicate that bifacial maps along the thalamocortical system do not offer a functional advantage. Instead, they lead to impairments, possibly due to the smaller size of the whisker-related modules and interference between the ipsilateral and contralateral whisker representations in the same thalamus and cortex. The whisker sensory system plays a quintessentially important role in exploratory behavior of mice and other nocturnal rodents. Here, we studied a novel mutant mouse line, in which the projections from the brainstem to the thalamus are disrupted. This led to formation of bilateral whisker maps in both the thalamus and the cortex. The two whisker maps crowd in a space normally devoted to the contralateral map alone and in a nonoverlapping fashion. Stimulation of the whiskers on either side activates the corresponding region of the map. Mice with bilateral whisker maps perform well in general sensorimotor tasks but show poor performance in specific tests that require whisker-dependent tactile discrimination. These observations indicate that contralateral, instead of bilateral, representation of the sensory space plays a critical role in acuity and fine discrimination during somesthesis.
Topics: Animals; Behavior, Animal; Exploratory Behavior; Female; Male; Mice; Mice, Inbred C57BL; Mice, Transgenic; Nerve Net; Psychomotor Performance; Somatosensory Cortex; Touch; Vibrissae
PubMed: 28663199
DOI: 10.1523/JNEUROSCI.0598-17.2017 -
Mechanisms of Development Nov 2006The development, maintenance and regeneration of epithelial appendages such as hairs or vibrissae depend on reciprocal interactions between the epidermal and the dermal...
The development, maintenance and regeneration of epithelial appendages such as hairs or vibrissae depend on reciprocal interactions between the epidermal and the dermal components of the integument. Growth factors are among a number of signaling molecules that have been identified during these developmental events. Growth factors such as fibroblast growth factors (FGFs) bind cell surface heparan sulfate proteoglycans (HSPGs) on their heparan sulfate side chains and as such these proteoglycans act as co-receptors for FGF receptors (FGFRs) by forming a ternary signaling complex of HSPG, FGFR and FGF. The syndecans make up a family (syndecan-1-4) of transmembrane HSPGs. In the present study we examined the growth response of mouse vibrissae to HSPG-binding growth factors as a function of the presence or absence of syndecan-4 in an organ culture system. Syndecan-4 is expressed on keratinocytes that make up the inner root sheath of the vibrissa. Vibrissae from wild-type mice, but not from syndecan-4 null mice, displayed a statistically significant and dose-dependent growth response to FGF-1, FGF-2 and FGF-7. In contrast, a statistically significant growth response is seen in vibrissae from both wild-type and syndecan-4 null mice when the culture medium is supplemented with either hepatocyte growth factor (HGF) that binds to HSPG, insulin that does not bind to HSPG or 5% fetal bovine serum. The syndecan-4 dependent effect of FGF-1, -2 and -7 on the transcriptional activity of IRS expressed genes and of genes involved in cell proliferation reveals a number of different response patterns. In vivo, the vibrissae of syndecan-4 null mice are shorter and have a smaller diameter than those of wild-type mice and this phenotype may result from a suboptimal response to growth factors. Syndecan-1, which is expressed in the outer root sheath of the vibrissae shaft, does not influence the response of the vibrissae to FGF-1, -2 and -7 and the length and diameter of vibrissae of syndecan-1 null mice do not differ from those of wild-type mice.
Topics: Animals; Fibroblast Growth Factors; Gene Expression Regulation, Developmental; Genotype; Mice; RNA, Messenger; Receptors, Fibroblast Growth Factor; Signal Transduction; Syndecan-4; Vibrissae
PubMed: 16989989
DOI: 10.1016/j.mod.2006.08.003 -
Journal of Neurophysiology Nov 2018Bodies change continuously, but we do not know if and how these changes affect somatosensory cortex. We address this issue in the whisker-barrel-cortex-pathway. We ask...
Bodies change continuously, but we do not know if and how these changes affect somatosensory cortex. We address this issue in the whisker-barrel-cortex-pathway. We ask how outgrowing whiskers are mapped onto layer 4 barrel neuron responses. Half of whisker follicles contained dual whiskers, a shorter presumably outgrowing whisker (referred to as young whisker) and a longer one (referred to as old whisker). Young whiskers were much thinner than old ones but were inserted more deeply into the whisker follicle. Both whiskers were embedded in one outer root sheath surrounded by a common set of afferent nerve fibers. We juxtacellularly identified layer 4 barrel neurons representing dual whiskers with variable whisker length differences in anesthetized rats. Strength and latency of neuronal responses were strongly correlated for deflections of young and old whiskers but were not correlated with whisker length. The direction preferences of young and old whiskers were more similar than expected by chance. Old whiskers evoked marginally stronger and slightly shorter latency spike and local field potential responses than young whiskers. Our data suggest a conservative rewiring mechanism, which connects young whiskers to existing peripheral sensors. The fact that layer 4 barrel neurons retain their response properties is remarkable given the different length, thickness, and insertion depth of young and old whiskers. Retention of cortical response properties might be related to the placement of young and old whisker in one common outer root sheath and may contribute to perceptual stability across whisker replacement. NEW & NOTEWORTHY A particularly dramatic bodily change is whisker regrowth, which involves the formation of dual whisker follicles. Our results suggest that both whiskers are part of the same mechanoreceptive unit. Despite their distinct whisker length and thickness, responses of single cortical neurons to young and old whisker deflection were similar in strength, latency, and directional tuning. We suggest the congruence of young and old whisker cortical responses contributes to perceptual stability over whisker regrowth.
Topics: Animals; Male; Rats; Rats, Long-Evans; Reaction Time; Sensory Receptor Cells; Somatosensory Cortex; Vibrissae
PubMed: 30044148
DOI: 10.1152/jn.00333.2018 -
Nature Communications Nov 2022Rodent sensory cortex contains salt-and-pepper maps of sensory features, whose structure is not fully known. Here we investigated the structure of the salt-and-pepper...
Rodent sensory cortex contains salt-and-pepper maps of sensory features, whose structure is not fully known. Here we investigated the structure of the salt-and-pepper whisker somatotopic map among L2/3 pyramidal neurons in somatosensory cortex, in awake mice performing one-vs-all whisker discrimination. Neurons tuned for columnar (CW) and non-columnar (non-CW) whiskers were spatially intermixed, with co-tuned neurons forming local (20 µm) clusters. Whisker tuning was markedly unstable in expert mice, with 35-46% of pyramidal cells significantly shifting tuning over 5-18 days. Tuning instability was highly concentrated in non-CW tuned neurons, and thus was structured in the map. Instability of non-CW neurons was unchanged during chronic whisker paralysis and when mice discriminated individual whiskers, suggesting it is an inherent feature. Thus, L2/3 combines two distinct components: a stable columnar framework of CW-tuned cells that may promote spatial perceptual stability, plus an intermixed, non-columnar surround with highly unstable tuning.
Topics: Mice; Animals; Vibrissae; Somatosensory Cortex; Neurons; Pyramidal Cells; Wakefulness; Rodentia
PubMed: 36329010
DOI: 10.1038/s41467-022-34261-1 -
Journal of Neurophysiology Apr 2021The rat whisker system connects the tactile environment with the somatosensory thalamocortical system using only two synaptic stages. Encoding properties of the first...
The rat whisker system connects the tactile environment with the somatosensory thalamocortical system using only two synaptic stages. Encoding properties of the first stage, the primary afferents with somas in the trigeminal ganglion (TG), has been well studied, whereas much less is known from the second stage, the brainstem trigeminal nuclei (TN). The TN are a computational hub giving rise to parallel ascending tactile pathways and receiving feedback from many brain sites. We asked the question, whether encoding properties of TG neurons are kept by two trigeminal nuclei, the principalis (Pr5) and the spinalis interpolaris (Sp5i), respectively giving rise to two "lemniscal" and two "nonlemniscal" pathways. Single units were recorded in anesthetized rats while a single whisker was deflected on a band-limited white noise trajectory. Using information theoretic methods and spike-triggered mixture models (STM), we found that both nuclei encode the stimulus locally in time, i.e., stimulus features more than 10 ms in the past do not significantly influence spike generation. They further encode stimulus kinematics in multiple, distinct response fields, indicating encoding characteristics beyond previously described directional responses. Compared with TG, Pr5 and Sp5i gave rise to lower spike and information rates, but information rate per spike was on par with TG. Importantly, both brainstem nuclei were found to largely keep encoding properties of primary afferents, i.e. local encoding and kinematic response fields. The preservation of encoding properties in channels assumed to serve different functions seems surprising. We discuss the possibility that it might reflect specific constraints of frictional whisker contact with object surfaces. We studied two trigeminal nuclei containing the second neuron on the tactile pathway of whisker-related tactile information in rats. We found that the subnuclei, traditionally assumed to give rise to functional tactile channels, nevertheless transfer primary afferent information with quite similar properties in terms of integration time and kinematic profile. We discuss whether such commonality may be due the requirement to adapt to physical constraints of frictional whisker contact.
Topics: Afferent Pathways; Animals; Biomechanical Phenomena; Electrophysiological Phenomena; Neurons, Afferent; Rats; Time Factors; Touch Perception; Trigeminal Nuclei; Vibrissae
PubMed: 33689491
DOI: 10.1152/jn.00350.2020 -
Advanced Science (Weinheim,... Jan 2023Seals can detect prey up to 180 m away using only their flow-sensing whiskers. The unique undulating morphology of Phocid seal whiskers reduces vortex-induced vibrations...
Seals can detect prey up to 180 m away using only their flow-sensing whiskers. The unique undulating morphology of Phocid seal whiskers reduces vortex-induced vibrations (VIVs), rendering seals highly sensitive to biologically relevant flow stimuli. In this work, digital models of harbor and grey seal whiskers are extracted using 3D scanning and a mathematical framework that accurately recreates their undulating geometry is proposed. Through fluid-structure interaction studies and experimental investigations involving a whisker array mounted on 3D-printed microelectromechanical systems sensors, the vibration characteristics of the whisker array and the interaction between neighboring whiskers in steady flows and fish-wake-like vortices are explained for the first time. Results reveal that the downstream vortices intensity and resulting VIVs are consistently lower for grey than harbor seal whiskers and a smooth cylinder, suggesting that the grey seal whisker geometry can be an ideal template for the biomimetic design of VIV-resistant underwater structures. In addition, neighboring whiskers in an array influence one another by resulting in greater flow vorticity fluctuation and distribution area, thus causing increased vibrations than an isolated whisker, which indicates the possibility of a signal-strengthening effect in whisker arrays.
Topics: Animals; Vibrissae; Hydrodynamics; Phoca; Vibration; Biomimetics
PubMed: 36403235
DOI: 10.1002/advs.202203062