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Neuron Apr 2016Sniffing and whisking typify the exploratory behavior of rodents. These actions involve separate oscillators in the medulla, located respectively in the pre-Bötzinger...
Sniffing and whisking typify the exploratory behavior of rodents. These actions involve separate oscillators in the medulla, located respectively in the pre-Bötzinger complex (preBötC) and the vibrissa-related region of the intermediate reticular formation (vIRt). We examine how these oscillators synergize to control sniffing and whisking. We find that the vIRt contains glycinergic/GABAergic cells that rhythmically inhibit vibrissa facial motoneurons. As a basis for the entrainment of whisking by breathing, but not vice versa, we provide evidence for unidirectional connections from the preBötC to the vIRt. The preBötC further contributes to the control of the mystacial pad. Lastly, we show that bilateral synchrony of whisking relies on the respiratory rhythm, consistent with commissural connections between preBötC cells. These data yield a putative circuit in which the preBötC acts as a master clock for the synchronization of vibrissa, pad, and snout movements, as well as for the bilateral synchronization of whisking.
Topics: Animals; Biological Clocks; GABAergic Neurons; Glycine; Motor Neurons; Neural Inhibition; Neural Pathways; Neurons; Periodicity; Rats; Respiration; Reticular Formation; Vibrissae
PubMed: 27041498
DOI: 10.1016/j.neuron.2016.03.007 -
Neuron Nov 2011An essential issue in perception is how the location of an object is estimated from tactile signals in the context of self-generated changes in sensor configuration.... (Review)
Review
An essential issue in perception is how the location of an object is estimated from tactile signals in the context of self-generated changes in sensor configuration. Here, we review the pathways and dynamics of neuronal signals that encode touch in the rodent vibrissa sensorimotor system. Rodents rhythmically scan an array of long, facial hairs across a region of interest. Behavioral evidence shows that these animals maintain knowledge of the azimuthal position of their vibrissae. Electrophysiological measurements have identified a reafferent signal of the azimuth that is coded in normalized coordinates, broadcast throughout primary sensory cortex and provides strong modulation of signals of vibrissa contact. Efferent signals in motor cortex report the range of the scan. Collectively, these signals allow the rodent to form a percept of object location.
Topics: Afferent Pathways; Animals; Brain Mapping; Humans; Neurons; Nonlinear Dynamics; Periodicity; Physical Stimulation; Somatosensory Cortex; Touch; Vibrissae
PubMed: 22078505
DOI: 10.1016/j.neuron.2011.10.009 -
The Journal of Neuroscience : the... Mar 2022Lateralization is a hallmark of somatosensory processing in the mammalian brain. However, in addition to their contralateral representation, unilateral tactile stimuli...
Lateralization is a hallmark of somatosensory processing in the mammalian brain. However, in addition to their contralateral representation, unilateral tactile stimuli also modulate neuronal activity in somatosensory cortices of the ipsilateral hemisphere. The cellular organization and functional role of these ipsilateral stimulus responses in awake somatosensory cortices, especially regarding stimulus coding, are unknown. Here, we targeted silicon probe recordings to the vibrissa region of primary (S1) and secondary (S2) somatosensory cortex of awake head-fixed mice of either sex while delivering ipsilateral and contralateral whisker stimuli. Ipsilateral stimuli drove larger and more reliable responses in S2 than in S1, and activated a larger fraction of stimulus-responsive neurons. Ipsilateral stimulus-responsive neurons were rare in layer 4 of S1, but were located in equal proportion across all layers in S2. Linear classifier analyses further revealed that decoding of the ipsilateral stimulus was more accurate in S2 than S1, whereas S1 decoded contralateral stimuli most accurately. These results reveal substantial encoding of ipsilateral stimuli in S1 and especially S2, consistent with the hypothesis that higher cortical areas may integrate tactile inputs across larger portions of space, spanning both sides of the body. Tactile information obtained by one side of the body is represented in the activity of neurons of the opposite brain hemisphere. However, unilateral tactile stimulation also modulates neuronal activity in the other, or ipsilateral, brain hemisphere. This ipsilateral activity may play an important role in the representation and processing of tactile information, in particular when the sense of touch involves both sides of the body. Our work in the whisker system of awake mice reveals that neocortical ipsilateral activity, in particular that of deep layer excitatory neurons of secondary somatosensory cortex (S2), contains information about the presence and the velocity of unilateral tactile stimuli, which supports a key role for S2 in integrating tactile information across both body sides.
Topics: Animals; Mammals; Mice; Somatosensory Cortex; Touch; Touch Perception; Vibrissae; Wakefulness
PubMed: 35135855
DOI: 10.1523/JNEUROSCI.1417-21.2022 -
Journal of Neurophysiology Jan 2012Rats generate stereotyped exploratory (5-12 Hz) vibrissa movements when navigating through their environment. Like other rhythmic behaviors, the production of whisking...
Rats generate stereotyped exploratory (5-12 Hz) vibrissa movements when navigating through their environment. Like other rhythmic behaviors, the production of whisking relies on a subcortical pattern generator. However, the relatively large vibrissae representation in motor cortex (vMCx) suggests that cortex also contributes to the control of whisker movements. The goal of this study was to examine the relationship between neuronal activity in vMCx and the kinematics of vibrissae movements. We recorded multiunit activity (MUA) and single units in the rhythmic region of vMCx while measuring vibrissa position in awake, head-restrained rats. The rats were engaged in one of two behavioral tasks where they were rewarded for either 1) producing noncontact whisking epochs that met specified criteria (epochs ≥4 Hz, whisks >5 mm) or 2) whisking to contact an object. There was significant coherence between the frequency of MUA and vibrissae movements during free-air whisking but not when animals were using their vibrissae to contact an object. Spike rate in vMCx was most frequently correlated with the amplitude of vibrissa movements; correlations with movement frequency did not exceed chance levels. These findings suggest that the specific parameter under cortical control may be the amplitude of whisker movements.
Topics: Action Potentials; Animals; Evoked Potentials, Motor; Female; Food Deprivation; Motor Cortex; Motor Neurons; Movement; Physical Stimulation; Rats; Rats, Long-Evans; Reaction Time; Spectrum Analysis; Statistics as Topic; Time Factors; Vibrissae
PubMed: 21994257
DOI: 10.1152/jn.01132.2010 -
Neuron May 2020To interpret the environment, our brain must evaluate external stimuli against internal representations from past experiences. How primary (S1) and secondary (S2)...
To interpret the environment, our brain must evaluate external stimuli against internal representations from past experiences. How primary (S1) and secondary (S2) somatosensory cortices process stimuli depending on recent experiences is unclear. Using simultaneous multi-area population imaging of projection neurons and focal optogenetic inactivation, we studied mice performing a whisker-based working memory task. We find that activity reflecting a current stimulus, the recollection of a previous stimulus (cued recall), and the stimulus category are distributed across S1 and S2. Despite this overlapping representation, S2 is important for processing cued recall responses and transmitting these responses to S1. S2 network properties differ from S1, wherein S2 persistently encodes cued recall and the stimulus category under passive conditions. Although both areas encode the stimulus category, only information in S1 is important for task performance through pathways that do not necessarily include S2. These findings reveal both distributed and segregated roles for S1 and S2 in context-dependent sensory processing.
Topics: Animals; Male; Memory, Short-Term; Mice; Models, Neurological; Neurons; Somatosensory Cortex; Touch Perception; Vibrissae
PubMed: 32164873
DOI: 10.1016/j.neuron.2020.02.004 -
The Journal of Comparative Neurology Jun 2021Barrel subfields in rodent primary somatosensory cortex (SI) are important model systems for studying cortical organization and reorganization. During cortical...
Barrel subfields in rodent primary somatosensory cortex (SI) are important model systems for studying cortical organization and reorganization. During cortical reorganization that follows limb deafferentation, neurons in deafferented forelimb SI become responsive to previously unexpressed inputs from the lower jaw. Although the lower jaw barrel subfield (LJBSF) is a likely source of the input, this subfield has received little attention. Our aim was to describe the structural and functional organization of the normal LJBSF. To investigate LJBSF organization, a nomenclature for lower jaw skin surface was developed, cytochrome oxidase (CO) was used to label flattened-cut LJBSF sections, microelectrodes were used to map the lower jaw skin surface representation in SI, and electrolytic lesions, recovered from electrode penetrations, were used to align the physiological map to the underlying barrel map. LJBSF is a tear-shaped subfield containing approximately 24 barrels, arranged in eight mediolateral rows and a barrel-free zone capping the anterior border. The representation of the lower jaw skin consisting of chin vibrissae and microvibrissae embedded in common fur is somatotopically organized in a single map in the contralateral SI. This physiological map shows that the activity from the vibrissae aligns with the CO-staining of the underlying LJBSF. LJBSF barrels receive topographically ordered barrel-specific input from individual vibrissa and microvibrissae in the lower jaw but not from trident whiskers. The barrel-free zone receives topographically ordered input from the lower lip. These data demonstrating that the LJBSF is a highly organized subfield are essential for understanding its possible role in cortical reorganization.
Topics: Animals; Brain Mapping; Female; Jaw; Neurons; Rats; Rats, Sprague-Dawley; Somatosensory Cortex; Vibrissae
PubMed: 33135168
DOI: 10.1002/cne.25063 -
The Journal of Neuroscience : the... Sep 2014When encountering novel environments, animals perform complex yet structured exploratory behaviors. Despite their typical structuring, the principles underlying...
When encountering novel environments, animals perform complex yet structured exploratory behaviors. Despite their typical structuring, the principles underlying exploratory patterns are still not sufficiently understood. Here we analyzed exploratory behavioral data from two modalities: whisking and locomotion in rats and mice. We found that these rodents maximized novelty signal-to-noise ratio during each exploration episode, where novelty is defined as the accumulated information gain. We further found that these rodents maximized novelty during outbound exploration, used novelty-triggered withdrawal-like retreat behavior, and explored the environment in a novelty-descending sequence. We applied a hierarchical curiosity model, which incorporates these principles, to both modalities. We show that the model captures the major components of exploratory behavior in multiple timescales: single excursions, exploratory episodes, and developmental timeline. The model predicted that novelty is managed across exploratory modalities. Using a novel experimental setup in which mice encountered a novel object for the first time in their life, we tested and validated this prediction. Further predictions, related to the development of brain circuitry, are described. This study demonstrates that rodents select exploratory actions according to a novelty management framework and suggests a plausible mechanism by which mammalian exploration primitives can be learned during development and integrated in adult exploration of complex environments.
Topics: Animals; Exploratory Behavior; Locomotion; Male; Mice; Models, Psychological; Rats; Vibrissae
PubMed: 25232104
DOI: 10.1523/JNEUROSCI.1872-14.2014 -
Journal of Neurophysiology Feb 1999The effects of C-fiber depletion induced by neonatal capsaicin treatment on the functional properties of vibrissa-sensitive low-threshold mechanoreceptive (LTM) neurons...
The effects of C-fiber depletion induced by neonatal capsaicin treatment on the functional properties of vibrissa-sensitive low-threshold mechanoreceptive (LTM) neurons in the rat trigeminal nucleus principalis were examined in adult rats. Neonatal rats were injected either with capsaicin or its vehicle within 48 h of birth. The depletion of unmyelinated afferents was confirmed by the significant decrease in plasma extravasation of Evan's blue dye induced in the hindlimb skin of capsaicin-treated rats by cutaneous application of mustard oil and by the significant decrease of unmyelinated fibers in both the sciatic and infraorbital nerves. The mechanoreceptive field (RF) and response properties of 31 vibrissa-sensitive neurons in capsaicin-treated rats were compared with those of 32 vibrissa-sensitive neurons in control (untreated or vehicle-treated) rats. The use of electronically controlled mechanical stimuli allowed quantitative analysis of response properties of vibrissa-sensitive neurons; these included the number of center- and surround-RF vibrissae within the RF (i.e., those vibrissae which when stimulated elicited >/=1 and <1 action potential per stimulus, respectively), the response magnitude and latency, and the selectivity of responses to stimulation of vibrissae in different directions with emphasis on combining both the response magnitude and direction of vibrissal deflection in a vector analysis. Neonatal capsaicin treatment was associated with significant increases in the total number of vibrissae, in the number of center-RF vibrissae per neuronal RF, and in the percentage of vibrissa-sensitive neurons that also responded to stimulation of other types of orofacial tissues. Compared with control rats, capsaicin-treated rats showed significant increases in the response magnitude to stimulation of surround-RF vibrissae as well as in response latency variability to stimulation of both center- and surround-RF vibrissae. C-fiber depletion also significantly altered the directional selectivity of responses to stimulation of vibrissae. For neurons with multiple center-RF vibrissae, the proportion of center-RF vibrissae with net vector responses oriented toward the same quadrant was significantly less in capsaicin-treated compared with control rats. These changes in the functional properties of principalis vibrissa-sensitive neurons associated with marked depletion of C-fiber afferents are consistent with similarly induced alterations in LTM neurons studied at other levels of the rodent somatosensory system, and indeed may contribute to alterations previously described in the somatosensory cortex of adult rodents. Furthermore, these results provide additional support to the view that C fibers may have an important role in shaping the functional properties of LTM neurons in central somatosensory pathways.
Topics: Animals; Animals, Newborn; Capsaicin; Evans Blue; Male; Mechanoreceptors; Mustard Plant; Nerve Fibers; Neurons; Plant Extracts; Plant Oils; Rats; Rats, Sprague-Dawley; Reaction Time; Trigeminal Nuclei; Vibrissae
PubMed: 10036296
DOI: 10.1152/jn.1999.81.2.435 -
Neuroscience Jan 2018After half a century of research, the sensory features coded by neurons of the rodent barrel cortex remain poorly understood. Still, views of the sensory representation... (Review)
Review
After half a century of research, the sensory features coded by neurons of the rodent barrel cortex remain poorly understood. Still, views of the sensory representation of whisker information are increasingly shifting from a labeled line representation of single-whisker deflections to a selectivity for specific elements of the complex statistics of the multi-whisker deflection patterns that take place during spontaneous rodent behavior - so called natural tactile scenes. Here we review the current knowledge regarding the coding of patterns of whisker stimuli by barrel cortex neurons, from responses to single-whisker deflections to the representation of complex tactile scenes. A number of multi-whisker tunings have already been identified, including center-surround feature extraction, angular tuning during edge-like multi-whisker deflections, and even tuning to specific statistical properties of the tactile scene such as the level of correlation across whiskers. However, a more general model of the representation of multi-whisker information in the barrel cortex is still missing. This is in part because of the lack of a human intuition regarding the perception emerging from a whisker system, but also because in contrast to other primary sensory cortices such as the visual cortex, the spatial feature selectivity of barrel cortex neurons rests on highly nonlinear interactions that remained hidden to classical receptive field approaches.
Topics: Animals; Rodentia; Somatosensory Cortex; Touch Perception; Vibrissae
PubMed: 28843997
DOI: 10.1016/j.neuroscience.2017.08.039 -
Developmental Dynamics : An Official... Feb 2010Somatosensation is the primary sensory modality employed by rodents in navigating their environments, and mystacial vibrissae on the snout are the primary conveyors of...
Somatosensation is the primary sensory modality employed by rodents in navigating their environments, and mystacial vibrissae on the snout are the primary conveyors of this information to the murine brain. The layout of vibrissae is spatially stereotyped and topographic connections faithfully maintain this layout throughout the neuraxis. Several factors have been shown to influence general vibrissal innervation by trigeminal neurons. Here, the role of a cell surface receptor, EphA4, in directing position-dependent vibrissal innervation is examined. EphA4 is expressed in the ventral region of the presumptive whisker pad and EphA4(-/-) mice lack the ventroposterior-most vibrissae. Analyses reveal that ventral trigeminal axons are abnormal, failing to innervate emerging vibrissae, and resulting in the absence of a select group of vibrissae in EphA4(-/-) mice. EphA4's selective effect on a subset of whiskers implicates cell-based signaling in the establishment of position-dependent connectivity and topography in the peripheral somatosensory system.
Topics: Animals; Axons; Gene Expression; Mice; Mice, Knockout; Receptor, EphA4; Signal Transduction; Trigeminal Nerve; Vibrissae
PubMed: 20014408
DOI: 10.1002/dvdy.22185