Thermal Stability of Contractile Proteins in Bat Wing Muscles Explains Differences in Temperature Dependence of Whole-Muscle Shortening Velocity.

AbstractMuscle contractile properties are dependent on temperature: cooler temperatures generally slow contractile rates. Contraction and relaxation are driven by underlying biochemical systems, which are inherently sensitive to temperature. Carollia perspicillata, a small Neotropical bat, experiences large temperature differentials among body regions, resulting in a steep gradient in temperature along the wing. Although the bats maintain high core body temperatures during flight, the wing muscles may operate at more than 10°C below body temperature. Partially compensating for these colder operating temperatures, distal wing muscles have lower temperature sensitivities in their contractile properties, including shortening velocity, relative to the proximal pectoralis. Shortening velocity is correlated with the activity of myosin ATPase, an enzyme that drives the cross-bridge cycle. We hypothesized that the thermal properties of myofibrillar ATPase from the pectoralis and forearm muscles of the bat wing would correlate with the temperature sensitivity of those muscles. Using myofibrillar ATPases from the proximal and distal muscles, we measured enzyme activity across a range of temperatures and enzyme thermal stability after heat incubation across a range of time points. We found that forearm muscle myofibrillar ATPase was significantly less thermally stable than pectoralis myofibrillar ATPase but that there was no significant difference in the acute temperature dependence of enzyme activity between the two muscles.

Muscle preactivation and the limits of muscle power output during jumping in the Cuban tree frog Osteopilus septentrionalis.

Previous studies of jumping in frogs have found power outputs in excess of what is possible from direct application of muscle power and concluded that jumping requires the storage and release of elastic strain energy. Of course, the muscles must produce the work required and their power output should be consistent with known muscle properties if the total duration of muscle activity is known. Using the Cuban tree frog, Osteopilus septentrionalis, I measured jumping performance from kinematics and used EMG measurements of three major jumping muscles to determine the duration of muscle activity. Using the total mass of all the hindlimb muscles, muscle mass-specific work output up to 60 J kg-1 was recorded. Distributed over the duration of the jump, both average and peak muscle mass-specific power output increased approximately linearly with the work done, reaching values of over 750 and 2000 W kg-1, respectively. However, the muscles were activated before the jump started. Both preactivation duration and EMG amplitude increased with increasing amounts of work performed. Assuming the muscles could produce work from EMG onset until toe-off, the average muscle mass-specific power over this longer interval also increased with work done, but only up to a work output of 36 J kg-1. The mean power above this value of work was 281 W kg-1, which is approximately 65% of the estimated maximum isotonic power. Several reasons are put forward for suggesting this power output, although within the known properties of the muscles, is nevertheless an impressive achievement.

A comparison of thermal sensitivities of wing muscle contractile properties from a temperate and tropical bat species.

Endotherms experience temperature variation among body regions, or regional heterothermy, despite maintaining high core body temperatures. Bat forelimbs are elongated to function as wings, which makes them vulnerable to heat loss and exaggerates regional heterothermy. A tropical bat species, Carollia perspicillata, flies with distal wing muscles that are substantially (>10°C) cooler than proximal wing muscles and significantly less temperature sensitive. We hypothesized that the difference between proximal and distal wing muscles would be even more extreme in a temperate bat species that is capable of flight at variable environmental temperatures. We measured the contractile properties of the proximal pectoralis muscle and distal extensor carpi radialis muscle at a range of temperatures in the big brown bat, Eptesicus fuscus, and compared their thermal dependence with that of the same muscles in C. perspicillata. We found that, overall, temperature sensitivities between species were remarkably similar. The sole exception was the shortening velocity of the pectoralis muscle in E. fuscus, which was less temperature sensitive than in C. perspicillata. This decreased temperature sensitivity in a proximal muscle runs counter to our prediction. We suggest that the relative lability of body temperature in E. fuscus may make better pectoralis function at low temperatures advantageous.

A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature.

The axial musculature of fishes has historically been characterized as the powerhouse for explosive swimming behaviors. However, recent studies show that some fish also use their 'swimming' muscles to generate over 90% of the power for suction feeding. Can the axial musculature achieve high power output for these two mechanically distinct behaviors? Muscle power output is enhanced when all of the fibers within a muscle shorten at optimal velocity. Yet, axial locomotion produces a mediolateral gradient of muscle strain that should force some fibers to shorten too slowly and others too fast. This mechanical problem prompted research into the gearing of fish axial muscle and led to the discovery of helical fiber orientations that homogenize fiber velocities during swimming, but does such a strain gradient also exist and pose a problem for suction feeding? We measured muscle strain in bluegill sunfish, Lepomis macrochirus, and found that suction feeding produces a gradient of longitudinal strain that, unlike the mediolateral gradient for locomotion, occurs along the dorsoventral axis. A dorsoventral strain gradient within a muscle with fiber architecture shown to counteract a mediolateral gradient suggests that bluegill sunfish should not be able to generate high power outputs from the axial muscle during suction feeding-yet prior work shows that they do, up to 438 W kg-1. Solving this biomechanical paradox may be critical to understanding how many fishes have co-opted 'swimming' muscles into a suction feeding powerhouse.

A proximal-distal difference in bat wing muscle thermal sensitivity parallels a difference in operating temperatures along the wing.

Flight is a demanding form of locomotion, requiring fast activation and relaxation in wing muscles to produce the necessary wingbeat frequencies. Bats maintain high body temperatures during flight, but their wing muscles cool under typical environmental conditions. Because distal wing muscles are colder during flight than proximal muscles, we hypothesized that they would be less temperature sensitive to compensate for temperature effects, resulting in proximal-distal differences in temperature sensitivity that match differences in muscle operating temperature. We measured contractile rates across temperatures in the proximal pectoralis muscle and an interosseous in the handwing of Carollia perspicillata, a small neotropical fruit bat, and compared their thermal dependence with that of a forearm muscle measured in a previous study. We found that the contractile properties of the pectoralis were significantly more temperature sensitive than those of the distal muscles. This suggests that cooling of the distal wing muscles imposes a selective pressure on muscle contractile function which has led to shifts in temperature sensitivity. This study is the first to demonstrate differences in temperature sensitivity along the length of a single limb in an endotherm and suggests that temperature variation may be underappreciated as a determinant of locomotor performance in endotherms generally.

The Multi-Scale, Three-Dimensional Nature of Skeletal Muscle Contraction.

Muscle contraction is a three-dimensional process, as anyone who has observed a bulging muscle knows. Recent studies suggest that the three-dimensional nature of muscle contraction influences its mechanical output. Shape changes and radial forces appear to be important across scales of organization. Muscle architectural gearing is an emerging example of this process.

Warm bodies, cool wings: regional heterothermy in flying bats.

Many endothermic animals experience variable limb temperatures, even as they tightly regulate core temperature. The limbs are often cooler than the core at rest, but because the large locomotor muscles of the limbs produce heat during exercise, they are thought to operate at or above core temperature during activity. Bats, small-bodied flying mammals with greatly elongated forelimbs, possess wings with large surfaces lacking any insulating fur. We hypothesized that during flight the relatively small muscles that move the elbow and wrist operate below core body temperature because of elevated heat loss. We measured muscle temperature continuously in the small fruit bat Carollia perspicillata before and during wind tunnel flights, and discretely in diverse bats at rest in Belize. We found that bats maintained high rectal temperatures, but that there was a steep proximal-to-distal gradient in wing muscle temperature. Forearm muscles were 4-6°C cooler than rectal temperature at rest and approximately 12°C cooler during flights at an air temperature of 22°C. These findings invite further study into how bats and other endotherms maintain locomotor performance in variable environments, when some muscles may be operating at low temperatures that are expected to slow contractile properties.

Low thermal dependence of the contractile properties of a wing muscle in the bat Carollia perspicillata.

Temperature affects contractile rate properties in muscle, which may affect locomotor performance. Endotherms are known to maintain high core body temperatures, but temperatures in the periphery of the body can fluctuate. Such a phenomenon occurs in bats, whose wing musculature is relatively poorly insulated, resulting in substantially depressed temperatures in the distal wing. We examined a wing muscle in the small-bodied tropical bat Carollia perspicillata and a hindlimb muscle in the laboratory mouse at 5°C intervals from 22 to 42°C to determine the thermal dependence of the contractile properties of both muscles. We found that the bat extensor carpi radialis longus had low thermal dependence from near body temperature to 10°C lower, with Q10 values of less than 1.5 for relaxation from contraction and shortening velocities in that interval, and with no significant difference in some rate properties in the interval between 32 and 37°C. In contrast, for all temperature intervals below 37°C, Q10 values for the mouse extensor digitorum longus were 1.5 or higher, and rate properties differed significantly across successive temperature intervals from 37 to 22°C. An ANCOVA analysis found that the thermal dependencies of all measured isometric and isotonic rate processes were significantly different between the bat and mouse muscles. The relatively low thermal dependence of the bat muscle likely represents a downward shift of its optimal temperature and may be functionally significant in light of the variable operating temperatures of bat wing muscles.

Speed of sound in muscle for use in sonomicrometry.

Converting ultrasound transit time into a measure of distance when using sonomicrometry requires that the speed of sound be known. A number of different values for the speed of sound in muscle have been assumed in studies of skeletal and cardiac muscle, and in some cases the effect of temperature has been ignored. The speed of ultrasound with frequencies greater than 1MHz in skeletal and cardiac muscle is briefly reviewed, including the effects of temperature and contractile state. A simplified equation for the speed of sound in pure water is presented for the temperature range from 0-50°C. This equation can be used when calibrating sonomicrometer transducers in water. The data available indicate that the speed of sound in both cardiac and skeletal muscle can be approximated by multiplying the speed of sound in pure water at the measurement temperature by 1.045. Differences in the speed of sound in the longitudinal and transverse directions and changes with contractile state appear to be small and in most cases can probably be safely ignored. The normal variation in muscle composition does not greatly affect the speed of ultrasound in muscle, but investigators placing sonomicrometer transducers near tendons should be conscious of the much greater speed of sound in tendon and variation with loading.

Judging the reality of others' memories.

Interpersonal reality monitoring (IRM) refers to our ability to evaluate whether other people's memories reflect real or imagined events. The current work examined IRM and whether or not it can be affected by training and feedback. We found that people are better than chance and that the ability to accurately make this judgement can be improved or reduced with appropriate and inappropriate training, respectively. Understanding IRM has implications for applied psychologists interested in how people evaluate others' descriptions of past events (e.g., eyewitness testimony).

The influence of mood on the process and content of encoding future intentions.

Remembering to perform an intention in the future when some environmental cue is encountered is referred to as event-based prospective memory. The influence of mood on this future-oriented memory is unclear. By experimentally manipulating mood, the current set of experiments sought to examine the influence that differing mood states have on encoding future intentions. Participants were induced into a neutral, positive, or negative mood state at intention formation and returned to their baseline mood before beginning the prospective memory task. Relative to the neutral mood, positive mood facilitated and negative mood impaired intention encoding when neutrally toned cues were used, as evidenced by the proportion of cues subsequently detected. The use of negatively toned cues ameliorated the benefit of the positive mood but not the impairment of the negative mood. Further, reinstatement of the encoding mood during retrieval equated performance for all three mood conditions. Results suggest that encoded mood influences the future accessibility and completion of intended behaviours, perhaps through modulation of associative processing. The current study demonstrates that mood plays a determining role in encoding future intentions.

Investigating the subjective reports of rejection processes in the word frequency mirror effect.

We sought to systematically investigate how participants subjectively classify the basis of their recognition memory judgments for low and high word frequency items. We found that participants more often reported rejection processes related to the increased perceived memorability for unstudied low word frequency items (relative to high word frequency items), rather than classifying their decision on a lack of familiarity. Experiment 2 replicated this pattern and demonstrated context variability and word frequency independently influenced the subjective classifications for correct rejections. Results of Experiment 3 revealed that these differences are dependent upon having experience with both low and high frequency items. Overall, these data suggest participants' rejection of low frequency items is more strongly related to judgments of perceived memorability, but only when they are presented in the context of high frequency items. The results are discussed in relation to distinctiveness and expected memorability.

Preparatory distributed cortical synchronization determines execution of some, but not all, future intentions.

Associating intentions to events that cue future behaviors is a central aspect of human cognition. There is limited understanding of the neural dynamics supporting recognition of intention-related events, with little known about how pre-event brain state varies as a function of intention specificity. Prior to recognized events (that cued planned behavior) occurring during an unrelated activity, we found increased steady-state visual evoked potential (ssVEP) and intrinsic gamma synchronization for ill- compared to well-specified events, as measured by EEG. Enhanced fronto-temporo-parietal ssVEP synchrony emerged preceding ill compared to well-specified events, and the degree of synchrony predicted the completion of ill-specified intentions but predicted failure to complete well-specified intentions. Distinct executive processing and neural states are therefore optimal for anticipating and fulfilling future intentions varying in event specificity.

Differential segmental strain during active lengthening in a large biarticular thigh muscle during running.

The iliotibialis lateralis pars postacetabularis (ILPO) is the largest muscle in the hindlimb of the guinea fowl and is thought to play an important role during the stance phase of running, both absorbing and producing work. Using sonomicrometry and electromyography, we examined whether the ILPO experiences differential strain between proximal, central and distal portions of the posterior fascicles. When the ILPO is being lengthened while active, the distal portion was found to lengthen significantly more than either the proximal or central portions of the muscle. Our data support the hypothesis that the distal segment lengthened farther and faster because it began activity at shorter sarcomere lengths on the ascending limb of the length-tension curve. Probably because of the self-stabilizing effects of operating on the ascending limb of the length-tension curve, all segments reached the end of lengthening and started shortening at the same sarcomere length. During shortening, this similarity in sarcomere length among the segments was maintained, as predicted from force-velocity effects, and shortening strain was similar in all segments. The differential active strain during active lengthening is thus ultimately determined by differences in strain during the passive portion of the cycle. The sarcomere lengths of all segments of the fascicles were similar at the end of active shortening, but after the passive portion of the cycle the distal segment was shorter. Differential strain in the segments during the passive portion of the cycle may be caused by differential joint excursions at the knee and hip acting on the ends of the muscle and being transmitted differentially by the passive visco-elastic properties of the muscle. Alternatively, the differential passive strain could be due to the action of active or passive muscles in the thigh that transmit force to the IPLO in shear. Based on basic sarcomere dynamics we predict that differential strain is more likely to occur in muscles undergoing active lengthening at the beginning of contraction than those undergoing only shortening.

Mechanisms producing coordinated function across the breadth of a large biarticular thigh muscle.

We examined the hypothesis that structural features of the iliotibialis lateralis pars postacetabularis (ILPO) in guinea fowl allow this large muscle to maintain equivalent function along its anterior-posterior axis. The ILPO, the largest muscle in the hindlimb of the guinea fowl, is a hip and knee extensor. The fascicles of the ILPO originate across a broad region of the ilium and ischium posterior to the hip. Its long posterior fascicles span the length of the thigh and insert directly on the patellar tendon complex. However, its anterior fascicles are shorter and insert on a narrow aponeurosis that forms a tendinous band along the anterior edge of the muscle and is connected distally to the patellar tendon. The biarticular ILPO is actively lengthened and then actively shortened during stance. The moment arm of the fascicles at the hip increases along the anterior to posterior axis, whereas the moment arm at the knee is constant for all fascicles. Using electromyography and sonomicrometry, we examined the activity and strain of posterior and anterior fascicles of the ILPO. The activation was not significantly different in the anterior and posterior fascicles. Although we found significant differences in active lengthening and shortening strain between the anterior and posterior fascicles, the differences were small. The majority of shortening strain is caused by hip extension and the inverse relationship between hip moment arm and fascicle length along the anterior-posterior axis was found to have a major role in ensuring similar shortening strain. However, because the knee moment arm is the same for all fascicles, knee flexion in early stance was predicted to produce much larger lengthening strains in the short anterior fascicles than our measured values at this location. We propose that active lengthening of the anterior fascicles was lower than predicted because the aponeurotic tendon of insertion of the anterior fascicles was stretched and only a portion of the lengthening had to be accommodated by the active muscle fascicles.

Function of a large biarticular hip and knee extensor during walking and running in guinea fowl (Numida meleagris).

Physiological and anatomical evidence suggests that in birds the iliotibialis lateralis pars postacetabularis (ILPO) is functionally important for running. Incorporating regional information, we estimated the mean sarcomere strain trajectory and electromyographic (EMG) amplitude of the ILPO during level and incline walking and running. Using these data and data in the literature of muscle energy use, we examined three hypotheses: (1) active lengthening will occur on the ascending limb of the length-tension curve to avoid potential damage caused by stretch on the descending limb; (2) the active strain cycle will shift to favor active shortening when the birds run uphill and shortening will occur on the plateau and shallow ascending limb of the length-tension curve; and (3) measures of EMG intensity will correlate with energy use when the mechanical function of the muscle is similar. Supporting the first hypothesis, we found that the mean sarcomere lengths at the end of active lengthening during level locomotion were smaller than the predicted length at the start of the plateau of the length-tension curve. Supporting the second hypothesis, the magnitude of active lengthening decreased with increasing slope, whereas active shortening increased. In evaluating the relationship between EMG amplitude and energy use (hypothesis 3), we found that although increases in EMG intensity with speed, slope and loading were positively correlated with muscle energy use, the quantitative relationships between these variables differed greatly under different conditions. The relative changes in EMG intensity and energy use by the muscle probably varied because of changes in the mechanical function of the muscle that altered the ratio of muscle energy use to active muscle volume. Considering the overall function of the cycle of active lengthening and shortening of the fascicles of the ILPO, we conclude that the function of active lengthening is unlikely to be energy conservation and may instead be related to promoting stability at the knee. The work required to lengthen the ILPO during stance is provided by co-contracting knee flexors. We suggest that this potentially energetically expensive co-contraction serves to stabilize the knee in early stance by increasing the mechanical impedance of the joint.

Divided attention interferes with fulfilling activity-based intentions.

Two experiments were conducted to examine the effects of divided attention on activity-based prospective memory. After establishing a goal to fulfill an intention upon completion of an ongoing activity, successful completion of the intention generally suffered when attention was being devoted to an additional task (Experiment 1). Forming an implementation intention at encoding ameliorated the negative effects of divided attention (Experiment 2). The results from the present experiments demonstrate that activity-based prospective memory is susceptible to distraction and that implementing encoding strategies that enhance prospective memory performance can reduce this interference. The current work raises interesting questions about the similarities and differences between event- and activity-based prospective memories.

On the role of imagery in event-based prospective memory.

The role of imagery in encoding event-based prospective memories has yet to be fully clarified. Herein, it is argued that imagery augments a cue-to-context association that supports event-based prospective memory performance. By this account, imagery encoding not only improves prospective memory performance but also reduces interference to intention-related information that occurs outside of context. In the current study, when lure words occurred outside of the appropriate responding context, the use of imagery encoding strategies resulted in less interference when compared with a standard event-based intention condition. This difference was eliminated when participants were not given a specific context to associate their intention (i.e., lures occurred within the appropriate responding context). These results support a cue-to-context association account of how imagery operates in certain event-based prospective memory tasks.

An observation on the spontaneous noticing of prospective memory event-based cues.

In event-based prospective memory, current theories make differing predictions as to whether intention-related material can be spontaneously noticed (i.e., noticed without relying on preparatory attentional processes). In 2 experiments, participants formed an intention that was contextually associated to the final phase of the experiment, and lures that overlapped to differing degrees with the features of the intention-related cues were embedded in the initial phase. When participants were outside of the appropriate responding context (i.e., the initial phase), they exhibited slower latencies to lures that exactly matched the features of their intention compared with other types of lures and control words. In addition, on a final remember/know recognition test, participants reported having greater subjective recollection for the occurrence of the exact-match lures. These results suggest that exact-match lures were spontaneously noticed and differentially processed in the absence of any observable preparatory attentional processes. The findings have implications for the theoretical debate over whether preparatory attention must always be relied upon to notice intention-related material.

The reactivation of associated information affects source monitoring.

In this study, we examined a source-monitoring phenomenon that arises from reactivated related information from the study phase. Three experiments showed that source attributions for target events were influenced not only by the target item itself, but also by studied information about related items. In Experiment 1, source memory for target items that have a high forward association value to a single related study item (e.g., credit) were affected by the source of the associated information (e.g., card), so that memory performance was better when associated items were presented in the same source rather than a different source. A similar effect occurred with bidirectional associates (Exp. 2), as well as with synonymous pairs of words (Exp. 3). We argue that the source information of the reactivated material can be commingled with information about a candidate during a source judgment at retrieval and thereby can affect performance.