Active sensation: insights from the rodent vibrissa sensorimotor system

Rats sweep their vibrissae through space to locate objects in their immediate environment. In essence, their view of the proximal world is generated through pliable hairs that tap and palpate objects. The texture and shape of those objects must be discerned for the rat to assess the value of the object. Furthermore, the location of those objects must be specified with reference to the position of the rat's head for the rat to plan its movements. Recent in vivo and in vitro electrophysiological measurements provide insight into the algorithms and mechanisms that underlie these behavioral-based computations.     

Active spatial perception in the vibrissa scanning sensorimotor system

Haptic perception is an active process that provides an awareness of objects that are encountered as an organism scans its environment. In contrast to the sensation of touch produced by contact with an object, the perception of object location arises from the interpretation of tactile signals in the context of the changing configuration of the body. A discrete sensory representation and a low number of degrees of freedom in the motor plant make the ethologically prominent rat vibrissa system an ideal model for the study of the neuronal computations that underlie this perception. We found that rats with only a single vibrissa can combine touch and movement to distinguish the location of objects that vary in angle along the sweep of vibrissa motion. The patterns of this motion and of the corresponding behavioral responses show that rats can scan potential locations and decide which location contains a stimulus within 150 ms. This interval is consistent with just one to two whisk cycles and provides constraints on the underlying perceptual computation. Our data argue against strategies that do not require the integration of sensory and motor modalities. The ability to judge angular position with a single vibrissa thus connects previously described, motion-sensitive neurophysiological signals to perception in the behaving animal.     

Translation of sensory input into behavioral output via an olfactory system

We investigate the logic by which sensory input is translated into behavioral output. First we provide a functional analysis of the entire odor receptor repertoire of an olfactory system. We construct tuning curves for the 21 functional odor receptors of the Drosophila larva and show that they sharpen at lower odor doses. We construct a 21-dimensional odor space from the responses of the receptors and find that the distance between two odors correlates with the extent to which one odor masks the other. Mutational analysis shows that different receptors mediate the responses to different concentrations of an odorant. The summed response of the entire receptor repertoire correlates with the strength of the behavioral response. The activity of a small number of receptors is a surprisingly powerful predictor of behavior. Odors that inhibit more receptors are more likely to be repellents. Odor space is largely conserved between two dissimilar olfactory systems.     

Variation in Young's modulus along the length of a rat vibrissa

Rats use specialized tactile hairs on their snout, called vibrissae (whiskers), to explore their surroundings. Vibrissae have no sensors along their length, but instead transmit mechanical information to receptors embedded in the follicle at the vibrissa base. The transmission of mechanical information along the vibrissa, and thus the tactile information ultimately received by the nervous system, depends critically on the mechanical properties of the vibrissa. In particular, transmission depends on the bending stiffness of the vibrissa, defined as the product of the area moment of inertia and Young's modulus. To date, Young's modulus of the rat vibrissa has not been measured in a uniaxial tensile test. We performed tensile tests on 22 vibrissae cut into two halves: a tip-segment and a base-segment. The average Young's modulus across all segments was 3.34±1.48GPa. The average modulus of a tip-segment was 3.96±1.60GPa, and the average modulus of a base-segment was 2.90±1.25GPa. Thus, on average, tip-segments had a higher Young's modulus than base-segments. High-resolution images of vibrissae were taken to seek structural correlates of this trend. The fraction of the cross-sectional area occupied by the vibrissa cuticle was found to increase along the vibrissa length, and may be responsible for the increase in Young's modulus near the tip.     

Neuronal basis for object location in the vibrissa scanning sensorimotor system

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.     

Organization of the sensory input of command neurons

Dynamics of habituation of synaptic responses to tactile stimulation of the snail skin was used as a criterion for defining organization of the receptive field of an escape behaviour command neurone. It was shown that every command neurone had its own specific nonhabituating area of the receptive field while the size of the field was common to all command neurones - it comprised the whole skin surface. The receptive field of a command neurone system is not homogeneous in structure. Areas corresponding to ecologically significant regions can be singled out by the maximal response amplitude and low rate of habituation.     

Subsurface tubular system in the outer sensory cells of the rat cochlea

Summary The system of subsurface tubules in the outer sensory cells of the rat cochlea consists of tubules lying immediately beneath the cell membrane. The tubules extend from the region below the cuticular plate, follow without interruption along the contours of the cell membrane, and terminate as a complicated, branched system under the nucleus. Several mitochondria are found on the cytoplasmic side of the tubules. Microtubules are observed in the space between the subsurface tubules and the mitochondria, in contact with the membranes of the subsurface system and, rarely, in contact with small, stalked vesicles.Current theories on the role of the subsurface system are discussed and a new one, considering possible involvement of the system in transport of the synaptic transmitter, is proposed.     

Cellular and extracellular involvement in the regeneration of the rat lower vibrissa follicle.

The sequence of events leading to the reconstruction of a fibre-producing hair follicle, after microsurgical amputation of the lower follicle bulb, has been detailed by immunohistology and electron microscopy. The initial response was essentially found to be a wound reaction, in that hyperproliferative follicle epidermis quickly spread to below the level of amputation--associated with downward movement of mesenchymal (or dermal) sheath cells. Fibronectin was prominent in both dermis and epidermis at this stage and, as in wound repair, preceded laminin and type IV collagen in covering the lower dermal-epidermal junction. Once a new basal line of epidermis and a complete basement membrane were established, laminin and type IV collagen were detected below this junction and within the prospective papilla-forming mesenchyme. This coincided with ultrastructural observations of profuse sub-basement membrane extracellular material in the region of new papilla formation. The glassy membrane displayed extensive ultrastructural modifications at its lower level, and these corresponded with localized variations in staining intensities for all three antibodies over time. The membrane hung below the level of the epidermis, and was crossed by migrating cells from the mesenchymal dermal sheath of the follicle - it acted to segregate the inner group of follicular dermal cells from wound fibroblasts. Extracellular matrix may be a mediator of the dermal-epidermal interactions associated with this hair follicle regeneration phenomenon.     

The sensory trigeminal system in birds: input, organization and effects of peripheral damage. A review.

The primary sensory trigeminal system in birds comprises the mesencephalic trigeminal nucleus and the trigeminal ganglion with projections to the principal sensory nucleus (PrV) and the descending tract with its subnuclei. Other cranial nerves can contribute to PrV and the descending system that together form the somatosensory system of the head. There is also a proprioceptive component. The somatosensory system comprises a component serving tactile sense and a nociceptive component. The former processes information from many mechanoreceptors in beak and tongue; both PrV and subnuclei of the descending system are involved. The nociceptive component consists of small ganglion cells projecting presumably to layers I and II of the caudal subnucleus of the descending trigeminal system and cervical dorsal horn; this is the only trigeminal region showing immunoreactivity for substance P. The effects of amputation of the tips of the beak of chickens (debeaking) are estimated by fiber counts in electron microscopic preparations of the trigeminal branches innervating that area, and by cell counts in Nissl stained sections of the trigeminal ganglion. Our data indicate that debeaking causes a loss of exteroceptive units, but not of nociceptive units. Comparison of sections stained for the presence of substance P (immunohistochemistry) did not reveal a long-term effect on the nociceptive system suggestive of the occurrence of chronic pain.     

The role of the ECoG theta- and alpha-frequency oscillations in rat vibrissa active movements

Characteristics of rat ECoG organization before and after vibrissa active movements were studied by means ofmicroelectrode recording. It was shown that different brain structures were recruited to a variable extent in planning and initiation of vibrissae active movements depending on a functional state.     

Bacillus subtilis two-component system sensory kinase DegS is regulated by serine phosphorylation in its input domain

Bacillus subtilis two-component system DegS/U is well known for the complexity of its regulation. The cytosolic sensory kinase DegS does not receive a single predominant input signal like most two-component kinases, instead it integrates a wide array of metabolic inputs that modulate its activity. The phosphorylation state of the response regulator DegU also does not confer a straightforward "on/off" response; it is fine-tuned and at different levels triggers different sub-regulons. Here we describe serine phosphorylation of the DegS sensing domain, which stimulates its kinase activity. We demonstrate that DegS phosphorylation can be carried out by at least two B. subtilis Hanks-type kinases in vitro, and this stimulates the phosphate transfer towards DegU. The consequences of this process were studied in vivo, using phosphomimetic (Ser76Asp) and non-phosphorylatable (Ser76Ala) mutants of DegS. In a number of physiological assays focused on different processes regulated by DegU, DegS S76D phosphomimetic mutant behaved like a strain with intermediate levels of DegU phosphorylation, whereas DegS S76A behaved like a strain with lower levels of DegU phophorylation. These findings suggest a link between DegS phosphorylation at serine 76 and the level of DegU phosphorylation, establishing this post-translational modification as an additional trigger for this two-component system.     

Linear and quadratic models of point process systems: Contributions of patterned input to output

In the 1880's Volterra characterised a nonlinear system using a functional series connecting continuous input and continuous output. Norbert Wiener, in the 1940's, circumvented problems associated with the application of Volterra series to physical problems by deriving from it a new series of terms that are mutually uncorrelated with respect to Gaussian processes. Subsequently, Brillinger, in the 1970's, introduced a point-process analogue of Volterra's series connecting point-process inputs to the instantaneous rate of point-process output. We derive here a new series from this analogue in which its terms are mutually uncorrelated with respect to Poisson processes. This new series expresses how patterned input in a spike train, represented by third-order cross-cumulants, is converted into the instantaneous rate of an output point-process. Given experimental records of suitable duration, the contribution of arbitrary patterned input to an output process can, in principle, be determined. Solutions for linear and quadratic point-process models with one and two inputs and a single output are investigated. Our theoretical results are applied to isolated muscle spindle data in which the spike trains from the primary and secondary endings from the same muscle spindle are recorded in response to stimulation of one and then two static fusimotor axons in the absence and presence of a random length change imposed on the parent muscle. For a fixed mean rate of input spikes, the analysis of the experimental data makes explicit which patterns of two input spikes contribute to an output spike.     

The role of sensory input in motor neuron sprouting control

Primary sensory neurons project to motor neurons directly or through interneurons and affect their activity. In our previous paper we showed that intramuscular sprouting can be affected by changing the sensory synaptic input to motor neurons. In this work, motor axon sprouting within a peripheral nerve (extramuscular sprouting) was induced by nerve injury at such a distance from muscle so as not to allow nerve-muscle trophic interactions. Two different procedures were carried out: (1) sciatic nerve crush and (2) sciatic nerve crush with homosegmental ipsilateral L3-L5 dorsal rhizotomy. The number of regenerating motor axons innervating extensor digitorum longus muscle was determined by in vivo muscle tension recordings and an index of their individual conduction rate was obtained by in vitro intracellular recordings of excitatory postsynaptic end-plate potentials in muscle fibers. The main findings were: (1) there are more regenerated axons distally from the lesion than parent axons proximally to the lesion (sprouting at the lesion); (2) sprouting at the lesion was negatively affected by homosegmental ipsilateral dorsal rhizotomy; (3) the number of motor axons innervating extensor digitorum longus muscle extrafusal fibers counted proximally to the lesion increased following nerve injury and regeneration but this did not occur when sensory input was lost. A transient innervation of extrafusal fibers by gamma motor neurons may explain the increase of motor axons counted proximally to the lesion.