Mechanism of polarized light perception.

As background for a report on our current selective adaptation experiments in decapod crustaceans, the various facts and hypotheses generally relevant to intraretinal sensitivity to polarized light in arthropods as well as cephalopods have been marshaled. On the basis of this review, the following working hypotheses have been made. 1) One ommatidium in the compound eye is the functional unit in image perception but contains in its component retinular cells subunits which can work independently in detecting other visual parameters, such as polarization. 2) Single retinular cells do respond differentially to light polarized in various planes. 3) Light sensitivity, including e-vector detection, is localized in the rhab domeres, which comprise closely packed arrays of microvilli protruding axially from retinular cells; the dichroism of the photopigment molecules, which are contained within the microvilli, provides the molecular basis of e-vector detection. 4) The visual pigment molecules have their major dichroic axis aligned predominantly parallel to the long axis of the microvillus containing them; typically all microvilli in a single rhab domere are closely parallel to one another, thus comprising at the cellular level a unit dichroic analyzer with maximum optical density to photons vibrating in the direction parallel to these microvillous protrusions. 5) In most decapod crustaceans, in cephalopods, and in some insects the microvilli in all rhabdomeres of a retinula are oriented in only two directions, perpendicular. to each other. Therefore, e-vector perception must depend at the retinular level on a two channel system consisting of a pair of dichroic analyzers with their major transmitting axes fixed at a 90 degrees angle determined by the two directions of microvillus orientation. Our new results on selective adaptation in the eye of Cardisoma provide direct experimental evidence for such a two-channel analyzer in which the pair of functional units have their maximum sensitivity to polarization in the same retinal directions as the rhab dom microvilli observed in electron micrographs. In turn, these directions correspond with the vertical and horizontal axes of the animal's normal spatial orientation. In e-vector detection the seven retinular cells of a single decapod ommatidium thus form two operational subgroups of four and three cells, respectively (39). The correspondence of the electrophysiological evidence for a dual polarization analyzer with the perpendicular directions shown by the microvilli in a single rhabdom strengthens the idea that one ommatidium is enough for detecting e-vector orientation. On this evidence we may conclude that the model developed above for a two-channel polarization analyzer effectively accounts for the relevant spectrophotometric, fine-structural, electrophysiological, and behavioral data currently available for a considerable number of arthropods and cephalopods.

Mechanical fatigue resistance of an implantable branched lead system for a distributed set of longitudinal intrafascicular electrodes.

OBJECTIVE: A neural interface system has been developed that consists of an implantable stimulator/recorder can with a 15-electrode lead that trifurcates into three bundles of five individual wire longitudinal intrafascicular electrodes. This work evaluated the mechanical fatigue resistance of the branched lead and distributed electrode system under conditions designed to mimic anticipated strain profiles that would be observed after implantation in the human upper arm. APPROACH: Custom test setups and procedures were developed to apply linear or angular strain at four critical stress riser points on the lead and electrode system. Each test was performed to evaluate fatigue under a high repetition/low amplitude paradigm designed to test the effects of arm movement on the leads during activities such as walking, or under a low repetition/high amplitude paradigm designed to test the effects of more strenuous upper arm activities. The tests were performed on representative samples of the implantable lead system for human use. The specimens were fabricated using procedures equivalent to those that will be used during production of human-use implants. Electrical and visual inspections of all test specimens were performed before and after the testing procedures to assess lead integrity. MAIN RESULTS: Measurements obtained before and after applying repetitive strain indicated that all test specimens retained electrical continuity and that electrical impedance remained well below pre-specified thresholds for detection of breakage. Visual inspection under a microscope at 10× magnification did not reveal any signs of damage to the wires or silicone sheathing at the stress riser points. SIGNIFICANCE: These results demonstrate that the branched lead of this implantable neural interface system has sufficient mechanical fatigue resistance to withstand strain profiles anticipated when the system is implanted in an arm. The novel test setups and paradigms may be useful in testing other lead systems.

A key to the classification of cutaneous mechanoreceptors.

The cutaneous mechanoreceptors of the cat can be assigned to one of 11 groups by using physiologic tests performed with hand-held stimulators. The method of classification is described, and the validity and utility of this classification scheme are discussed.

Metallized polymer fibers as leadwires and intrafascicular microelectrodes.

We have developed a process for producing fine, very flexible microwires suitable for use as small signal leadwires or nerve electrodes. The process incorporates metallization of high-performance monofilament polymer fibers to yield electrically conductive fibers with greatly improved flexibility over solid metal wires of similar strength. The metallization layers are produced by serial vacuum deposition of a 0.3 micron thick coating of three metals, titanium-tungsten (Ti/W), gold (Au), and platinum (Pt), onto monofilament, poly-p-phenyl-terephthalate aramid fibers (Kevlar). The metallized fibers are then insulated with an approx. 1 micron thick layer of silicone elastomer. The result is a microlead with high electrical conductivity (linear resistance = 30 omega/cm), desirable interfacial properties, excellent mechanical stability and extremely high flexibility. These physical characteristics are appropriate for application as signal leadwires or recording/stimulating electrodes where small size and high flexibility are paramount. In this paper we report on the electrical and mechanical properties of these metallized fibers and demonstrate their use as intrafascicular electrodes for recording multi-unit neural activity in feline peripheral nerves.

Ascending collaterals of cutaneous neurons in the fasciculus gracilis of the cat during peripheral nerve regeneration.

Dorsal column projection patterns and conduction velocities of regenerating myelinated sensory neurons were studied at intervals between 1 and 12 months after transection of the sural nerve. The neurons had significantly decreased conduction velocities, both in the fasciculus gracilis and in the periphery. Although dorsal root reflexes were temporarily abolished, there was no evidence of gross rearrangement of the neurons' ascending collaterals in the dorsal columns in response to transection of their peripheral processes or as a result of reestablishment of functional peripheral connections. These findings support the hypothesis that when a regenerating cutaneous sensory neuron reforms functional peripheral connections in tissue it originally innervated, its receptor properties are similar to those it had before the nerve was lesioned.

Effect of activation and adaptation on the sensitivity of slowly adapting cutaneous mechanoreceptors.

The effect of adaptation on the sensitivity of type I and type II cutaneous mechanoreceptors was evaluated with test stimuli applied before, during and after a persistent indentation (offset) of the skin. It was found that the offset initially lowered the threshold to both high (100-200 Hz) and low (1-20 Hz) frequency sinusoidal stimuli, as compared with the preoffset condition. This lowered threshold increased for both stimuli as adaptation progressed. When adaptation was nearly complete, there was an appreciable residual reduction of threshold, as compared with preoffset values, for the low frequency stimuli but not for high frequency stimuli. For a time after the offset was removed, the threshold was increased above preoffset levels for both stimuli. Suprathreshold ramp displacements superimposed on an offset caused higher maximal frequencies and a larger change in frequency than before the offset was applied. This difference often was considerable (20-40 impulses/sec) even though the discharge produced by the offset had adapted to only 2-4 impulses/sec above the preoffset level. Shortly after removal of the offset, the ramp responses typically were less than before the offset was applied. Thus, these receptors are not "reset" to the preoffset condition by adaptation nor is their sensitivity reduced. On the contrary, they respond more vigorously to superimposed stimuli except for near threshold displacements that are brief and rapid.

Ascending collaterals of cutaneous neurons in the fasciculus gracilis of the cat.

Primary sensory neurons with myelinated axons in the sural nerve of the cat were found to be divisible into 3 systems on the basis of the length of their central collaterals in the dorsal columns. The short system consists of neurons that ascend only a segment or two in the fasciculus gracilis above their level of entry into the spinal cord. It is composed of all neurons with peripheral conduction velocities in the Adelta range and thus includes both D hair and nociceptive neurons. Approximately 35% of the Aalpha neurons join the intermediate system and ascend 4-12 segments before leaving the forsal columns. This system is composed of all sural type I neurons, as well as about 40% of the G2 hair, 40% of the intermediate field, and 50% of the F2 field neurons in the nerve. Those nociceptive neurons conducting at Aalpha velocities also contribute to the intermediate system. The remaining G2 hair, intermediate field, and F2 field neurons, together with almost all the sural type II, G1 hair, intermediate hair and F1 field neurons, join the long system and ascend to the nucleus gracilis. Fibers in the intermediate system showed a relatively abrupt decrease in conduction velocity usually of 50% or more (median 71%) a few millimeters rostral to their entry into the spinal cord. Members of the long system also decreased in conduction velocity at this point, but the magnitude of the changes was typically less than 50% of the peripheral velocity (median 36%). In addition, the ascending collaterals of the long system underwent a second reduction in conduction velocity near the cervical enlargement.

Rapid displacements of the skin lack clear positional information.

Rapid skin indentations can produce strong tap-like sensations that contain little information about skin indentation depth. Although slower stimuli produce weaker sensations, subjects can more accurately identify how the position of the skin surface changes with respect to the deeper tissues. This dissociation between intensity and depth information suggests that intensity and depth are served by different neural circuits.

Mobility performance with a pixelized vision system.

A visual prosthesis, based on electrical stimulation of the visual cortex, has been suggested as a means for partially restoring functional vision in the blind. The prosthesis would create a pixelized visual sense consisting of punctate spots of light (phosphenes). The present study investigated the feasibility of achieving visually-guided mobility with such a visual sense. Psychophysical experiments were conducted on normally sighted human subjects, who were required to walk through a maze which included a series of obstacles, while their visual input was restricted to information from a pixelized vision simulator. Walking speed and number of body contacts with obstacles and walls were measured as a function of pixel number, pixel spacing, object minification, and field of view. The results indicate that a 25 x 25 array of pixels distributed within the foveal visual area could provide useful visually guided mobility in environments not requiring a high degree of pattern recognition.

A quantitative evaluation of suture and tubulization nerve repair techniques.

The radial and sural nerves in cats were transected and either left unrepaired, repaired with 11-0 epineurial sutures, sutured and treated with topical application of Kenalog, or tubulated with hypoantigenic collagen. One year later the nerves were examined electrophysiologically, using single unit recording techniques, and histologically, by light microscopy. The results indicate that regeneration through the neuroma was comparable in all four groups, but that reinnervation of sensory structures in the skin was most successful in the tubulated nerves.

Action potential classification with dual channel intrafascicular electrodes.

Using recordings of peripheral nerve activity made with carbon fiber intrafascicular electrodes, we compared the performance of three different recording techniques (single channel, differential, and dual channel) and four different unit classification methods (linear discriminant analysis, template matching, a novel time amplitude windowing technique, and neural networks) in terms of errors in waveform classification and artifact rejection. Dual channel recording provided uniformly superior unit separability, neural networks gave the lowest classification error rates, and template matching had the best artifact rejection performance.

Separation of action potentials in multiunit intrafascicular recordings.

Classification of action potentials in multiunit recordings was based on the use of various types of features to uniquely characterize action potentials from different cells. We compared classification results obtained using three types of descriptive features: digitized data points, amplitude and duration (time domain) parameters, and fast Fourier transform (FFT) coefficients. Digitized data points used as descriptive features provided good classification success and required minimal computation. Time-domain features gave comparable results but required more computation. FFT coefficients were less effective than the other features. As the signal-to-noise ratio of the recordings increased, smaller differences in feature values could be discriminated.

Information contained in sensory nerve recordings made with intrafascicular electrodes.

Multiunit recordings were made in anesthetized cats with chronically implanted intrafascicular electrodes over a period of six months. Neural signals recorded with these electrodes consisted of activity in sensory fibers innervating a variety of cutaneous mechanoreceptors. Mechanical stimuli were used to selectively activate individual nerve fibers, and the receptive field and receptor type were identified for each unit. Over a period of six months, there was a net shift in the recorded population, but the electrodes continued to provide a representative sample of the activity in the fascicle as a whole. The total number of units from which activity could be recorded remained roughly constant with time, and individual units persisted in the recordings for up to six months. These results indicate that intrafascicular electrodes could be used to sample information carried by individual somatosensory fibers on a long term basis.

A silicon-based, three-dimensional neural interface: manufacturing processes for an intracortical electrode array.

A method has been developed for the manufacture of a "three-dimensional" electrode array geometry for chronic intracortical stimulation. This silicon based array consists of a 4.2 x 4.2 x 0.12 mm thick monocrystalline substrate, from which project 100 conductive, silicon needles sharpened to facilitate cortical penetration. Each needle is electrically isolated from the other needles, and is about 0.09 mm thick at its base and 1.5 mm long. The sharpened end of each needle is coated with platinum to facilitate charge transfer into neural tissue. The following manufacturing processes were used to create this array. 1) Thermomigration of 100 aluminum pads through an n-type silicon block. This creates trails of highly conductive p+ silicon isolated from each other by opposing pn junctions. 2) A combination of mechanical and chemical micromachining which creates individual penetrating needles of the p+ silicon trails. 3) Metal deposition to create active electrode areas and electrical contact pads. 4) Array encapsulation with polyimide. The geometrical, mechanical, and electrical properties of these arrays should make them well suited as interfaces to cortical tissue.

Analysis of single-unit firing patterns in multi-unit intrafascicular recordings.

A system for extracting single-unit activity patterns from multi-unit neural recordings was tested using real and simulated neural data. The system provided reliable estimates of firing frequency for individual units in simulated multi-unit data and allowed reliable determinations of the responses of individual cutaneous mechanoreceptor units to 'natural' stimuli such as brushing or pressing on the skin. An implementation of the system, which operated online and in real time, was used to obtain estimates of multiple, single-unit responses from multi-unit intrafascicular electrode recordings. The pattern of activity across the population of units in a given recording gave a reliable indication of the type of stimulus that had evoked the activity. It was concluded that this system, used in combination with intrafascicular peripheral nerve recordings, could be used to provide online, real-time information about peripheral stimuli.

Effects of short-term training on sensory and motor function in severed nerves of long-term human amputees.

Much has been studied and written about plastic changes in the CNS of humans triggered by events such as limb amputation. However, little is known about the extent to which the original pathways retain residual function after peripheral amputation. Our earlier, acute study on long-term amputees indicated that central pathways associated with amputated peripheral nerves retain at least some sensory and motor function. The purpose of the present study was to determine if these functional connections would be strengthened or improved with experience and training over several days time. To do this, electrodes were implanted within fascicles of severed nerves of long-term human amputees to evaluate the changes in electrically evoked sensations and volitional motor neuron activity associated with attempted phantom limb movements. Nerve stimulation consistently resulted in discrete, unitary, graded sensations of touch/pressure and joint-position sense. There was no significant change in the values of stimulation parameters required to produce these sensations over time. Similarly, while the amputees were able to improve volitional control of motor neuron activity, the rate and pattern of change was similar to that seen with practice in normal individuals on motor tasks. We conclude that the central plasticity seen after amputation is most likely primarily due to unmasking, rather than replacement, of existing synaptic connections. These results also have implications for neural control of prosthetic limbs.

Selective activation of muscle groups in the feline hindlimb through electrical microstimulation of the ventral lumbo-sacral spinal cord.

Selective activation of muscle groups in the feline hindlimb by electrical stimulation of the ventral lumbo-sacral spinal cord was investigated. Spinal cord segments L5 to S1 were mapped using a penetrating tungsten needle electrode. Locations that produced isolated contraction of quadriceps, tibialis anterior or triceps surae/plantaris muscles when stimulated with a current of 40 microA or less, and in which spread of activity to other muscles was not detected after increasing the stimulus to at least twice the threshold level, were defined as belonging to the target muscle's "activation pool." The quadriceps activation pool was found to extend from the beginning of L5 to the middle of L6. The tibialis anterior activation pool extended from the beginning of L6 to the middle of L7, and the triceps surae/plantaris activation pool extended from the caudal end of L6 to the beginning of S1. The three activation pools were located in Rexed motor lamina IX and their spatial organization was found to correspond well with that of the anatomically defined motor pools innervating the same muscles. The spatial and functional segregation of motor pools manifested at the spinal cord level can have direct applications in the areas of functional electrical stimulation and motor control.