Blockage of vibrissae afferents: II. Footshock threshold increments

Because of their dense innervation rat vibrissae have been regarded as a very important sensory system. Many behavioral deficits have been reported by other authors after rat vibrissal afferent blockades. In the present work we found significant threshold increments to footshock following either reversible nerve block (procaine or nerve pressure) or section of the vibrissal afferent nerves, but not following vibrissae trimming. These results are discussed in reference to the tonic or level-setting function of afferent systems.     

Chemoanatomical separation of vibrissal trigeminal primary afferents in the rat: a special central representation of supraorbital vibrissae

A choleratoxin B subunit transganglionic labelling technique and NPY immunohistochemistry were applied in the rat to achieve the chemoanatomical separation of myelinated vibrissal primary afferents, previously considered to be morphologically indistinguishable. Further, a special central representation pattern of supraorbital vibrissae was observed in the trigeminal brainstem nuclear complex: (1) Choleratoxin-labelled supraorbital vibrissal primary afferents terminated densely in their appropriate barrelettes in the trigeminal principal sensory nucleus, in the spinal oral subnucleus, in the caudal part of the spinal interpolar subnucleus, and in lamina IV of the caudal part of the spinal caudal subnucleus. (2) A second population of choleratoxin-labelled vibrissal afferents was also observed, terminating only in lamina III of the caudal subnucleus. (3) After peripheral nerve transection, NPY-immunoreactive supraorbital vibrissal primary afferent fibres appeared in their appropriate barrelettes in the principal sensory nucleus and the caudal part of the interpolar subnucleus, while in the caudal part of the caudal subnucleus NPY-immunoreactive vibrissal primary afferent terminals were found exclusively in the inner part of lamina II, extending over the outer part of lamina III. NPY-immunoreactive supraorbital vibrissal primary afferents were never found in the oral subnucleus. In contrast with the rules of the central representation of the mystacial (infraorbital) vibrissae, the multiple representation of the supraorbital vibrissae in the caudal subnucleus and the dense, barrelette-like terminal arborization of the choleratoxin-labelled supraorbital vibrissal primary afferents in the oral subnucleus apparently indicate an enhanced role of supraorbital vibrissae in reflexes that protect the eyes and the head from damage.     

Innervation patterns of mystacial vibrissae support active touch behaviors in California sea lions (Zalophus californianus)

Vibrissae or follicle-sinus complexes (F-SCs) are highly developed mammalian sensory structures. These blood-filled sinuses are richly innervated and possess novel mechanoreceptors. Although much is known regarding the function of F-SCs in terrestrial mammals, much less is known regarding marine carnivores such as pinnipeds. Pinnipeds possess the largest, most highly innervated vibrissae of any mammal. One such pinniped is the California sea lion, which are generalist marine predators that rely heavily upon tactile discrimination capabilities. Psychophysical studies demonstrate that haptic tactile discrimination using F-SCs is exceptionally sensitive. However, our knowledge of the structure and function of F-SCs in otariids is limited. Our objectives were to investigate the innervation and microstructure of F-SCs across the mystacial vibrissal field and infer function from haptic performance studies in California sea lions. Innervation and microstructure of vibrissae differed considerably compared to similar data available for phocids. Total innervation of mystacial vibrissae was estimated to be 86,042 axons. Investigations of innervation density and investment of microvibrissae versus macrovibrissae demonstrated a significantly increased axon density per F-SC in medial microvibrissal regions compared to lateral macrovibrissae, which supports psychophysical data and somatotopic organization of the central nervous system involved with tactile discrimination capability. Innervation increased from medial microvibrissae (705 ± 125 axons/F-SC) to lateral macrovibrissae (1,447 ± 154) as well as from dorsal (541 ± 60) to ventral (1,493 ± 327) vibrissal regions. These data provide a more complete picture of the sensory ecology of this important aquatic mammalian lineage; the specialization of peripheral sensory structures, central nervous structures with demonstrated enhanced haptic capabilities behaviorally has likely led to the ecological success of California sea lions.     

Fused traditional and geometric morphometrics demonstrate pinniped whisker diversity

Vibrissae (whiskers) are important components of the mammalian tactile sensory system, and primarily function as detectors of vibrotactile information from the environment. Pinnipeds possess the largest vibrissae among mammals and their vibrissal hair shafts demonstrate a diversity of shapes. The vibrissae of most phocid seals exhibit a beaded morphology with repeating sequences of crests and troughs along their length. However, there are few detailed analyses of pinniped vibrissal morphology, and these are limited to a few species. Therefore, we comparatively characterized differences in vibrissal hair shaft morphologies among phocid species with a beaded profile, phocid species with a smooth profile, and otariids with a smooth profile using traditional and geometric morphometric methods. Traditional morphometric measurements (peak-to-peak distance, crest width, trough width and total length) were collected using digital photographs. Elliptic Fourier analysis (geometric morphometrics) was used to quantify the outlines of whole vibrissae. The traditional and geometric morphometric datasets were subsequently combined by mathematically scaling each to true rank, followed by a single eigendecomposition. Quadratic discriminant function analysis demonstrated that 79.3, 97.8 and 100% of individuals could be correctly classified to their species based on vibrissal shape variables in the traditional, geometric and combined morphometric analyses, respectively. Phocids with beaded vibrissae, phocids with smooth vibrissae, and otariids each occupied distinct morphospace in the geometric morphometric and combined data analyses. Otariids split into two groups in the geometric morphometric analysis and gray seals appeared intermediate between beaded- and smooth-whiskered species in the traditional and combined analyses. Vibrissal hair shafts modulate the transduction of environmental stimuli to the mechanoreceptors in the follicle-sinus complex (F-SC), which results in vibrotactile reception, but it is currently unclear how the diversity of shapes affects environmental signal modulation.     

Neural encoding schemes of tactile information in afferent activity of the vibrissal system

When rats acquire sensory information by actively moving their vibrissae, a neural code is manifested at different levels of the sensory system. Behavioral studies in tactile discrimination agree that rats can distinguish different roughness surfaces by whisking their vibrissae. The present study explores the existence of neural encoding in the afferent activity of one vibrissal nerve. Two neural encoding schemes based on “events” were proposed (cumulative event count and median inter-event time). The events were detected by using an event detection algorithm based on multiscale decomposition of the signal (Continuous Wavelet Transform). The encoding schemes were quantitatively evaluated through the maximum amount of information which was obtained by the Shannon’s mutual information formula. Moreover, the effect of difference distances between rat snout and swept surfaces on the information values was also studied. We found that roughness information was encoded by events of 0.8 ms duration in the cumulative event count and event of 1.0 to 1.6 ms duration in the median inter-event count. It was also observed that an extreme decrease of the distance between rat snout and swept surfaces significantly reduces the information values and the capacity to discriminate among the sweep situations.     

The contribution of afferent signals from the liver to metabolic regulation during exercise

The crucial role of the liver as the only organ to produce glucose used by skeletal muscle during exercise is well known. Since hepatic glucose production is central to blood glucose homeostasis during exercise, it has been postulated that the liver may inform the central nervous system and other organs of its diminishing capacity to produce glucose from glycogen, before blood glucose falls. The sensory role of the liver during exercise would be similar to its role in the control of food intake. As a consequence, the experimental approaches used to test the hypothesis that afferent signals from the liver contribute to metabolic regulation during exercise are inspired by those used to test the same hypothesis in the regulation of food intake. In the present review, two questions are addressed. The existing evidence for the liver's sensory influence on metabolic adjustments to exercise is first reviewed; the nature of the initiating stimuli for the afferent contribution of the liver to physical exercise is discussed thereafter. The hypothetical construct upon which rests the contribution of the liver's afferent signals to metabolic regulation during exercise is that a decrease in liver glycogen or a related metabolic intermediate is sensed by the liver, and the signal is transduced to the central nervous system, most likely through the afferent activity of the hepatic vagus nerve, where it contributes to the orchestration of the metabolic and hormonal responses to exercise. Support in favour of this construct comes mainly from the demonstration that sectioning of the hepatic vagus nerve attenuates the normal hormonal response to exercise. It seems that the liver-glucagon axis is particularly responsive to this reflex activation. In other respects, the hepatic mechanism responsible for linking the metabolic activity in the liver to an afferent signal capable of regulating the metabolic response to exercise remains speculative. Substrates or derivatives of substrate oxidation, energy-related compounds (ATP and Pi), or changes in cell volume may all be related to changes in transmembrane potential in the liver cell, which according to the "potentiostatic" theory would determine the afferent vagal activity.     

Flow sensing by pinniped whiskers

Beside their haptic function, vibrissae of harbour seals (Phocidae) and California sea lions (Otariidae) both represent highly sensitive hydrodynamic receptor systems, although their vibrissal hair shafts differ considerably in structure. To quantify the sensory performance of both hair types, isolated single whiskers were used to measure vortex shedding frequencies produced in the wake of a cylinder immersed in a rotational flow tank. These measurements revealed that both whisker types were able to detect the vortex shedding frequency but differed considerably with respect to the signal-to-noise ratio (SNR). While the signal detected by sea lion whiskers was substantially corrupted by noise, harbour seal whiskers showed a higher SNR with largely reduced noise. However, further analysis revealed that in sea lion whiskers, each noise signal contained a dominant frequency suggested to function as a characteristic carrier signal. While in harbour seal whiskers the unique surface structure explains its high sensitivity, this more or less steady fundamental frequency might represent the mechanism underlying hydrodynamic reception in the fast swimming sea lion by being modulated in response to hydrodynamic stimuli impinging on the hair.     

Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats

Peripheral sensory organs provide the first transformation of sensory information, and understanding how their physical embodiment shapes transduction is central to understanding perception. We report the characterization of surface transduction during active sensing in the rodent vibrissa sensory system, a widely used model. Employing high-speed videography, we tracked vibrissae while rats sampled rough and smooth textures. Variation in vibrissa length predicted motion mean frequencies, including for the highest velocity events, indicating that biomechanics, such as vibrissa resonance, shape signals most likely to drive neural activity. Rough surface contact generated large amplitude, high-velocity "stick-slip-ring" events, while smooth surfaces generated smaller and more regular stick-slip oscillations. Both surfaces produced velocities exceeding those applied in reduced preparations, indicating active sensation of surfaces generates more robust drive than previously predicted. These findings demonstrate a key role for embodiment in vibrissal sensing and the importance of input transformations in sensory representation.     

An internal model architecture for novelty detection: implications for cerebellar and collicular roles in sensory processing

The cerebellum is thought to implement internal models for sensory prediction, but details of the underlying circuitry are currently obscure. We therefore investigated a specific example of internal-model based sensory prediction, namely detection of whisker contacts during whisking. Inputs from the vibrissae in rats can be affected by signals generated by whisker movement, a phenomenon also observable in whisking robots. Robot novelty-detection can be improved by adaptive noise-cancellation, in which an adaptive filter learns a forward model of the whisker plant that allows the sensory effects of whisking to be predicted and thus subtracted from the noisy sensory input. However, the forward model only uses information from an efference copy of the whisking commands. Here we show that the addition of sensory information from the whiskers allows the adaptive filter to learn a more complex internal model that performs more robustly than the forward model, particularly when the whisking-induced interference has a periodic structure. We then propose a neural equivalent of the circuitry required for adaptive novelty-detection in the robot, in which the role of the adaptive filter is carried out by the cerebellum, with the comparison of its output (an estimate of the self-induced interference) and the original vibrissal signal occurring in the superior colliculus, a structure noted for its central role in novelty detection. This proposal makes a specific prediction concerning the whisker-related functions of a region in cerebellar cortical zone A(2) that in rats receives climbing fibre input from the superior colliculus (via the inferior olive). This region has not been observed in non-whisking animals such as cats and primates, and its functional role in vibrissal processing has hitherto remained mysterious. Further investigation of this system may throw light on how cerebellar-based internal models could be used in broader sensory, motor and cognitive contexts.     

Why the ovotestis of Helix aspersa is innervated

Although Schmalz described the innervation of the ovotestis in pulmonate snails as early as 1914, no functions have been attributed to it. In H. aspersa, the intestinal nerve branches profusely within the ovotestis and terminates in the walls of the acini and in the sheath surrounding the early portion of the hermaphroditic duct. We found both sensory and motor functions for this innervation. Significantly, there is a tonic sensory discharge generated by the mechanical pressure of growing oocytes, and the level of tonic afferent activity is strongly correlated with the number of ripe oocytes; this is probably a permissive signal that gates ovulation. Tactile stimulation of the ovotestis causes a phasic sensory discharge and a pronounced cardio activation. Also, an efferent discharge is elicited in the ovotestis branch of the intestinal nerve. To study the motor consequences of efferent activity, the ovotestis branch was electrically stimulated. We found that such stimulation evokes peristaltic contractions of the initial portion of the hermaphroditic duct and increases beat frequencies of the cilia that line the interior of the duct. These effects could facilitate the transport of oocytes down the duct. Still other functions of afferent activity are implied by changes in the spontaneous activity of mesocerebral cells following nerve stimulation. Putative sensory neurons and putative motoneurons have been identified in the visceral and right parietal ganglia.     

Regulation of afferent transmission in the feeding circuitry of Aplysia

Although feeding in Aplysia is mediated by a central pattern generator (CPG), the activity of this CPG is modified by afferent input. To determine how afferent activity produces the widespread changes in motor programs that are necessary if behavior is to be modified, we have studied two classes of feeding sensory neurons. We have shown that afferent-induced changes in activity are widespread because sensory neurons make a number of synaptic connections. For example, sensory neurons make monosynaptic excitatory connections with feeding motor neurons. Sensori-motor transmission is, however, regulated so that changes in the periphery do not disrupt ongoing activity. This results from the fact that sensory neurons are also electrically coupled to feeding interneurons. During motor programs sensory neurons are, therefore, rhythmically depolarized via central input. These changes in membrane potential profoundly affect sensori-motor transmission. For example, changes in membrane potential alter spike propagation in sensory neurons so that spikes are only actively transmitted to particular output regions when it is behaviorally appropriate. To summarize, afferent activity alters motor output because sensory neurons make direct contact with motor neurons. Sensori-motor transmission is, however, centrally regulated so that changes in the periphery alter motor programs in a phase-dependent manner.     

Encoding of vibrissal active touch

Mammals acquire much of their sensory information by actively moving their sensory organs. Yet, the principles of encoding by active sensing are not known. Here we investigated the encoding principles of active touch by rat whiskers (vibrissae). We induced artificial whisking in anesthetized rats and recorded from first-order neurons in the trigeminal ganglion. During active touch, first-order trigeminal neurons presented a rich repertoire of responses, which could not be inferred from their responses to passive deflection stimuli. Individual neurons encoded four specific events: whisking, contact with object, pressure against object, and detachment from object. Whisking-responsive neurons fired at specific deflection angles, reporting the actual whiskers' position with high precision. Touch-responsive neurons encoded the horizontal coordinate of objects' position by spike timing. These findings suggest two specific encoding-decoding schemes for horizontal object position in the vibrissal system.     

A combined electrophysiological and behavioural study for the assessment of activity-dependent changes in mice

Activity-dependent adaptive changes in the nervous system involve structural and functional changes in the cortical circuitry. In this work the cortical function was studied by repeated recording of the somatosensory and motor potentials evoked by whisker deflections after altered sensory-motor experience in adult mice. The latencies of motor and somatosensory evoked potentials were found to shorten, while their amplitudes decreased, after a behavioural challenge involving the vibrissal apparatus. Sensory deprivation achieved by whisker trimming resulted in a partial reversal of the changes observed after increased activity. The derived parameters imply that cortical information processing speeds up as a result of experience, while decreased activity has the opposite effect. The methods used throughout the experiment were minimally invasive, and thus proved to be sufficient for the long-term follow-up of cortical functions.     

Axon typing of rat muscle nerves using a double staining procedure for cholinesterase and carbonic anhydrase.

We developed a method for detecting activity of axonal cholinesterase (CE) and carbonic anhydrase (CA)--markers for motor and sensory nerve fibers (NFs)--in the same histological section. To reach this goal, cross-sections of muscle nerves were sequentially incubated with the standard protocols for CE and CA histochemistry. A modified incubation medium was used for CA in which Co++ is replaced by Ni++. This avoids interference of the two histochemical reactions because Co++ binds unspecifically to the brown copper-ferroferricyanide complex representing CE activity, whereas Ni++ does not. Cross-sections of the trapezius muscle nerve containing efferent and afferent NFs in segregated fascicles showed that CE activity was confined to motor NFs. Axonal CA was detected solely in sensory NFs. The number of labeled motor and sensory NFs determined in serial cross-sections stained with either the new or the conventional technique was not significantly different. Morphometric analysis revealed that small unreactive NFs (diameter less than 5 microns) are afferent, medium-sized ones (5 microns less than d less than 7 microns) are unclassifiable, and large ones (d greater than 7 microns) are efferent. The heterogenous CE activity of thick (alpha) motor NFs is linked to the type of their motor units. "Fast" motor units contain CE reactive NFs; "slow" ones have CE negative neurites.     

Afferent inhibition and functional properties of neurons in the vibrissae projection area of the cat somatosensory cortex]

The aim of this study was to investigate the role of inhibitory processes in S-1 cortex of cats. The inhibition was evoked by "natural" afferent stimulation of the fascial vibrissae. For this purpose, two neighboring vibrissae were sequentially stimulated by mechanical deflection; single unit activity was recorded simultaneously from the cortex. Results showed that conditioning by afferent stimulation significantly influenced the directional sensitivity of cortical neurons. These data and analysis of spatial pattern of stimulated vibrissa indicate that detector neurons could be quickly modified during sensory processing.     

Serotonin and motor activity

The activity of brain serotonergic neurons in both the pontine-mesencephalic and medullary groups is positively correlated with the level of behavioral arousal and/or the behavioral state. This, in turn, appears to be related to the level of tonic motor activity, especially as manifested in antigravity muscles and other muscle groups associated with gross motor activity. In addition, a subset of serotonergic neurons displaysa further increase in activity in association with repetitive, central pattern generator mediated responses. Accumulating evidence indicates that this relation to motor activity is related both to the co-activation of the sympathetic nervous system and to the modulation of afferent inputs.     

Effects and consequences of nerve injury on the electrical properties of sensory neurons

Nociceptive pain alerts the body to potential or actual tissue damage. By contrast, neuropathic or "noninflammatory" pain, which results from injury to the nervous system, serves no useful purpose. It typically continues for years after the original injury has healed. Sciatic nerve lesions can invoke chronic neuropathic pain that is accompanied by persistent, spontaneous activity in primary afferent fibers. This activity, which reflects changes in the properties and functional expression of Na+, K+, and Ca2+ channels, initiates a further increase in the excitability of second-order sensory neurons in the dorsal horn. This change persists for many weeks. The source of origin of the pain thus moves from the peripheral to the central nervous system. We hypothesize that this centralization of pain involves the inappropriate release of peptidergic neuromodulators from primary afferent fibers. Peptides such as substance P, neuropeptide Y (NPY), calcitonin-gene-related peptide (CGRP), and brain-derived neurotrophic factor (BDNF) may promote enduring changes in excitability as a consequence of neurotrophic actions on ion channel expression in the dorsal horn. Findings that form the basis of this hypothesis are reviewed. Study of the neurotrophic control of ion channel expression by spinal peptides may thus provide new insights into the etiology of neuropathic pain.     

Histological changes in the somatosensory thalamus after unilateral coagulation of vibrissa follicles of the muzzle of the newborn mouse

Light microscopic study of the thalamic ventro-basal complex (VB), after unilateral coagulation of vibrissae follicles in newborn mouse, revealed an excess of neuronal perikarya on the controlateral "deafferented" side as compared to the normal side. The higher density of nerve cells was confined to the vibrissal relay in the medial part of VB nucleus (VBm), whereas the cell number in the non vibrissal-lateral part of this nucleus (VB1) remained on the control level. Electron microscopic investigation of the thalamic vibrissal relay has shown signs of a modified synaptogenesis on the "deafferented" side: (a) the number of specific afferents has diminished and in contrast to the normal side, most of the specific sensory terminals contain small spheroid synaptic vesicles and (b) the number of axon terminals with ovoid pleomorphic vesicles has been doubled.     

Innervation of the maxillary vibrissae in mice as revealed by anterograde and retrograde tract tracing

Vibrissae are a unique sensory system of mammals that is characterized by a rich and diverse innervation involved in numerous sensory tasks with the potential for species-specific differences. In the present study, indocarbocyanine dyes (DiI and PTIR271) and confocal microscopy were combined to study the innervation of the mystacial vibrissae and vibrissa-specific sensory neuron distribution in the maxillary portion of the trigeminal ganglion of the mouse. The deeper regions of the vibrissa cavernous sinus (CS) contained a dense plexus of free nerve endings, possibly of autonomic fibers. The superficial part of this sinus displayed a massive array of corpuscular endings. Innervation in the region of the ring sinus consisted of Merkel endings and different morphological variances of lanceolate endings. The region of the inner conical body had a circular plexus of free nerve endings. In addition to confirming previous observations obtained by a variety of other techniques and ultrastructural studies, our studies revealed denser terminal receptor endings in a different distribution pattern than previously demonstrated in studies using the rat. We also revealed the distribution of sensory neurons in the trigeminal ganglion using retrograde tracing with fluorescent tracers from two nearby vibrissae. We determined that the populations of sensory neurons innervating the two vibrissae were largely overlapping. This suggests that the somatotopic maps of vibrissal projections reported at the different levels in the neuraxis are not faithfully reproduced at the level of the ganglion.This work was supported by a grant from the NIDCD (RO1 DC 005590; BF), the Egyptian government (AM), and the NIH (ES00365-01 and RR-02-003; LH).     

The morphology of the rat vibrissal array: a model for quantifying spatiotemporal patterns of whisker-object contact

In all sensory modalities, the data acquired by the nervous system is shaped by the biomechanics, material properties, and the morphology of the peripheral sensory organs. The rat vibrissal (whisker) system is one of the premier models in neuroscience to study the relationship between physical embodiment of the sensor array and the neural circuits underlying perception. To date, however, the three-dimensional morphology of the vibrissal array has not been characterized. Quantifying array morphology is important because it directly constrains the mechanosensory inputs that will be generated during behavior. These inputs in turn shape all subsequent neural processing in the vibrissal-trigeminal system, from the trigeminal ganglion to primary somatosensory ("barrel") cortex. Here we develop a set of equations for the morphology of the vibrissal array that accurately describes the location of every point on every whisker to within ±5% of the whisker length. Given only a whisker's identity (row and column location within the array), the equations establish the whisker's two-dimensional (2D) shape as well as three-dimensional (3D) position and orientation. The equations were developed via parameterization of 2D and 3D scans of six rat vibrissal arrays, and the parameters were specifically chosen to be consistent with those commonly measured in behavioral studies. The final morphological model was used to simulate the contact patterns that would be generated as a rat uses its whiskers to tactually explore objects with varying curvatures. The simulations demonstrate that altering the morphology of the array changes the relationship between the sensory signals acquired and the curvature of the object. The morphology of the vibrissal array thus directly constrains the nature of the neural computations that can be associated with extraction of a particular object feature. These results illustrate the key role that the physical embodiment of the sensor array plays in the sensing process.