John P. Schroeter

Role of the Z band in the mechanical properties of the heart.

In striated muscle the mechanism of contraction involves the cooperative movement of contractile and elastic components. This review emphasizes a structural approach that describes the cellular and extracellular components with known anatomical, biochemical, and physical properties that make them candidates for these contractile and elastic components. Classical models of contractile and elastic elements and their underlying assumptions are presented. Mechanical properties of cardiac and skeletal muscle are compared and contrasted and then related to ultrastructure. Information from these approaches leads to the conclusion that the Z band is essential for muscle contraction. Our review of Z band structure shows the Z band at the interface where extracellular components meet the cell surface. The Z band is also the interface from cell surface to myofibril, from extramyofibrillar to myofibril, and finally from sarcomere to sarcomere. Our studies of Z band in defined physiologic states show that this lattice is an integral part of the contractile elements and can function as an elastic component. The Z band is a complex dynamic lattice uniquely suited to play several roles in muscle contraction.—Goldstein, M. A.; Schroeter, J. P.; Michael, L. H. Role of the Z band in the mechanical properties of the heart. FASEB J. 5: 2167–2174; 1991.

Z band dynamics as a function of sarcomere length and the contractile state of muscle.

The Z band in skeletal muscle has two distinct structural states —a relaxed (small square or ss) form and a maximally activated (basket weave or bw) form. We have examined by electron microscopy and optical diffraction Z lattice forms and dimensions and A band spacings in relaxed, tetanized, stretched, and stretched‐and‐tetanized rat soleus muscle. We have tested the independent contributions of passive load, active tension, and sarcomere length to Z band state. As the A band spacing decreased with increasing load and increasing sarcomere length in the untetanized muscles, the Z lattice remained in the ss form and the Z spacing changed only slightly. Computer‐enhanced images from digitized electron micrographs showed that the ss Z lattice resisted deformation regardless of load or method of stretching. In contrast, when the muscle was tetanized at sarcomere lengths of up to 2.7 μm, the Z lattice assumed the bw form and the Z spacing was increased by 20%. Regardless of lattice form, Z spacing did not vary significantly with sarcomere length. Images from freeze‐substituted preparations showed both lattice forms comparable to those in images from glutaraldehyde‐fixed muscles. Thus, Z band state appears to be a function of the presence (or absence) of active tension. Our previous three‐dimensional model is compatible with these observations and with the substructures revealed by computer‐enhanced images of both lattice forms.—Goldstein, M. A.; Michael, L. H.; Schroeter, J. P.; Sass, R. L. Z band dynamics as a function of sarcomere length and the contractile state of muscle. FASEB J. 1: 133‐142; 1987.

The Z-band lattice in skeletal muscle before, during and after tetanic contraction

SummaryElectron micrographs and optical diffraction patterns of the Z-band were studied in rat soleus muscle fixed before, during, and after tetanic contraction. We compared the morphology (small square or basketweave pattern) and dimensions of the Z-lattice of control and tetanized muscles near rest length. Z-bands of muscle fixed at rest and of muscle allowed to rest after a tetanic contraction exhibited the small square pattern. Z-bands from muscle fixed during tetanic contraction exhibited the basketweave pattern. Concomitant with the transition to basketweave, we observed an average increase of 20% in spacing between the axial filaments of the Z-lattice. Optical diffraction measurements of the A-bandd10 spacing revealed that the Z/A ratio remained constant during the transition. We have modelled the small square to basketweave transformation as resulting from a change of curvature of constant length cross-connecting Z-filaments when the axial filaments increase their separation.

The Z-band lattice in a slow skeletal muscle

SummaryStructural features of the Z-lattice were examined in cross-sections of rat soleus muscle. Optical diffraction analysis of individual myofilament bundles revealed highly ordered, tightly packed tetragonal lattice regions with abrupt shifts in orientation. Optical reconstructions of cross-sections of the Z-lattice in regions having the same axial filament spacing showed both the basket weave and the small square lattice forms, as well as intermediate structures. Analysis of these regions in three dimensions and in two-dimensional projections suggests that a change in diameter together with a change in curvature of the cross-connecting filaments can explain the different appearances of the Z-lattice at a given sarcomere length.

Polarization contrast and motion detection

Form and motion perception rely upon the visual system’s capacity to segment the visual scene based upon local differences in luminance or wavelength. It is not clear if polarization contrast is a sufficient basis for motion detection. Here we show that crayfish optomotor responses elicited by the motion of images derived from spatiotemporal variations in e-vector angles are comparable to contrast-elicited responses. Response magnitude increases with the difference in e-vector angles in adjacent segments of the scene and with the degree of polarization but the response is relatively insensitive to the absolute values of e-vector angles that compose the stimulus. The results indicate that polarization contrast can support visual motion detection.

Optical reconstruction of nemaline rods

Abstract Optically filtered and reconstructed images were obtained from the Z lattice in a specimen of partially extracted skeletal muscle from a patient with nemaline myopathy. Data from longitudinal sections of Z rods showed a 37.5-nm repeat along the axial filaments associated with an array of connecting filaments. Projected distances between axial filaments were consistent with a 25-nm centered square array in cross sections. Data from longitudinal sections of glycerinated rabbit psoas muscle and normal rat soleus muscle showed a similar repeating unit. Optical reconstructions revealed differences in the substructure of the Z lattice, but similar unit cell dimensions in all three cases.

Visual Responses of Crayfish Ocular Motoneurons: An Information Theoretical Analysis

Motoneuron responses were elicited by global visual motion and stepwise displacements of an illuminated stripe. Stimulus protocols were identical to those used in previous behavioral studies of compensatory eyestalk reflexes. The firing rates and directional selectivity of the motoneuron responses were measured with respect to four stimulus dimensions (spatial frequency, contrast, angular displacement and velocity). The directional selectivity of the motoneuron response was correlated to the previously measured gain of the reflex for each stimulus dimension. The information theoretical analysis is based upon Kullback-Leibler (K-L) distances which measure the dissimilarity of responses to different stimuli. K-L distances for single neurons are strongly influenced by the mean rate difference of the responses to any pair of stimuli. Because of redundancy, the joint K-L distances of pairs of neurons were less than the sum of the K-L distances of the individual neurons. Furthermore, the joint K-L distances were only weakly influenced by correlations among coactivated neurons. For most of the stimulus dimensions, the K-L distances of single motoneurons were not sufficient to account for the stimulus discriminations exhibited by the eyestalk reflex which typically required the summed output of 2 to 5 motoneurons. Thus the behaviorally relevant information is encoded in the motoneuron ensemble. The minimum time required to discriminate the direction of motion (the encoding window) for a single motoneuron is about 380 to 480 ms (including a 175 ms response latency) for stepwise displacements and up to 1.0 s for global motion. During this period a motoneuron fires 2 to 3 impulses.

Visual Signals in an Optomotor Reflex: Systems and Information Theoretic Analysis

Compensatory optomotor reflexes were examined in crayfish (Procambarus clarkii) with oscillating sine wave gratings and step displacements of a single stripe. A capacitance transducer was used to measure the rotation of the eyestalk about its longitudinal axis. System studies reveal a spatial frequency response independent of velocity and stimulus amplitude and linear contrast sensitivity similar to that of neurons in the visual pathway. The reflex operates at low temporal frequencies (<0.002 Hz to 0.5 Hz) and exhibits a low-pass temporal frequency response with cut-off frequency of 0.1 Hz. Eyestalk rotation increases as a saturable function of the angular stimulus displacement. When compared to the oscillatory response, transient responses are faster, and they exhibit a lower gain for large stimulus displacements. These differences may reflect system nonlinearity and/or the presence of at least two classes of afferents in the visual pathway. Our metric for information transmission is the Kullback-Leibler (K-L) distance, which is inversely proportional to the probability of an error in distinguishing two stimuli. K-L distances are related to differences in responsiveness for variations in spatial frequency, contrast, and angular displacement. The results are interpreted in terms of the neural filters that shape the system response and the constraints that the K-L distances place on information transmission in the afferent visual pathway.

Orientation by polarized light in the crayfish dorsal light reflex: behavioral and neurophysiological studies

In decapod crustaceans, the dorsal light reflex rotates the eyestalk so that the dorsal retina faces the brightest segment of dorsal visual space. Stepwise displacements of white stripes elicit eyestalk rotations in the same direction as that of the stripe. Conversely, stepwise displacements of black stripes on a white background elicit eyestalk rotations in the opposite direction as that of the stripe. The reversal of the response with contrast inversion distinguishes the dorsal light reflex from an optokinetic reflex. When the visual scene is composed of polarized light, segmented by variations in e-vector orientation, displacement of segments containing near vertical e-vectors elicit responses similar to those elicited by a white stripe. Displacement of polarized stripes containing near horizontal e-vectors elicit eyestalk rotations similar to those elicited by a black stripe. The results are consistent with the use of polarized light in orientation. The stimulus conditions described above were also applied to visual interneurons (sustaining fibers) and oculomotor neurons and the results were generally in accord with the behavior. In the neural studies, it was possible to show that responses to polarized stripe displacements are predictable from the receptive field location and the neuron’s polarization tuning function.

The Z-band lattice in skeletal muscle in rigor

Previous work with tetanized and relaxed muscle has shown a correlation between active tension and the structure of the Z-band. This suggests that there is a correlation between the cross-bridge binding in the A-band and the structure of the Z-band. Using electron microscopy and optical diffraction we have examined this correlation in glycerinated muscle in rigor and in unstimulated intact muscle. We have found that the Z-bands of muscles in rigor always show the basketweave form, while those of the unstimulated muscles always show the small square form. The basketweave form found in rigor muscles is similar in form and dimension to that found in tetanized muscle. Thus it appears that the small square form of the Z-band is found in physiological states with little cross-bridge binding and the basketweave form is found in states with a high degree of cross-bridge binding.