The presented study investigated the dynamics and kinematics during the manually tested AF utilizing a handheld device in healthy participants under the influence of neutral, pleasant or disgusting odors, respectively. The evaluation of the slope of force rises reveal a non-significant difference between the three odors. Accordingly, the following discussion is based on reliable force applications of the testers. The main outcomes are:
The maximum AF (AFmax) does not differ significantly between the three odors. The main difference is that smelling neutral and pleasant odors, the AFmax was reached under isometric conditions (AFisomax), whereas with disgusting odor, the AFmax was obtained during muscle lengthening (AFeccmax). The AFisomax was significantly lower by perceiving disgusting compared to pleasant and neutral odors, indicating that during disgusting odor, the participants merged into eccentric muscle action at a significantly lower force level (60% of AFeccmax), whereas under neutral or pleasant olfactory influence isometric stability was maintained almost until the maximum. That confirms the hypothesis that the maximal isometric AF, but not the AFmax, decreases during perception of a disgusting odor.
The AF at the oscillation onset is significantly lower for neutral and pleasant compared to disgusting odor, in which no or only poor oscillations occurred at a high force level. This indicates that the AF in healthy persons perceiving neutral or pleasant odors is characterized by oscillations, which emerge during force rise at 75% of the maximum.
The testers’ force profile application might be the main limitation in this investigation. As mentioned above, the force application must be reproducible and appropriate as suggested in36. A smooth start followed by a faster linear force increase might be suitable to test the adaptive capability of the neuromuscular system36. The testers proofed their ability to test reproducibly prior to the investigation and the slope was used as parameter to control the force increase. The slopes did not differ significantly in the present measurements between the MMTs with different odors. The slope prior to the breaking point is even slightly lower in measurement with disgusting compared to pleasant odor (-3%). This speaks against the frequently appearing criticism that an unstable MMT is due to a steeper force rise. Nevertheless, the slope might be one crucial parameter when applying the force rise and must be controlled. An assessment of the force application by recording the dynamics and kinematics during MMT should take place to verify reliable and valid results.
Furthermore, the reached maximum force of a stable muscle depends not only on the participant, but also on the tester. The force profile is a result of their interaction. Because the participant is only reacting in a holding way, the tester determines the course of force including its maximum when a stable muscle is tested. That is why it depends on the tester to what extend the participant´s holding capability is challenged under stable conditions. Due to biomechanical aspects, it is mostly not possible to overcome the here tested rectus femoris and biceps brachii muscles. However, if the tester applies a lower maximum force, the participant’s response will naturally be lower, too. Therefore, the AFmax does not reflect the real maximum strength of the participant, since it depends on the amount of force applicated by the tester. As mentioned above, the “break test” is characterized by a force application in submaximal areas. However, the AFisomax under unstable conditions will refer to the maximal holding AF under the obviously impairing influence of a disgusting odor. The AFeccmax monitors the maximal eccentric force of the participants under the given circumstances. Since the AFisomax under stable conditions and the AFeccmax under unstable conditions are not differing significantly in the present study, it is assumable the applied force of the tester is close to the maximal force capacity of the participants; with the assumption that the AFeccmax is not changed by the influence of disgusting olfaction. Since the MMT was performed in submaximal areas, no statement can be made concerning the behavior of AFeccmax under the effect of neutral or pleasant odors. This investigation remains.
A tendency of a lower AFmax is visible for the tests under stable (neutral/pleasant) compared to unstable conditions (disgusting) (Figure 6A). This could be comprehended as a possible reason for the different muscle states. However, the decisive difference is that the breaking point (AFisomax) in unstable conditions (disgusting) appeared at a substantially and significantly lower level compared to the maximum force the muscle reached under stable conditions (neutral/pleasant) without muscle lengthening.
Another limitation is the small sample size (n = 10). However, the significances and effect sizes are considerably high. That is why we regard these preliminary results as a valuable first consideration reflecting the neuromuscular control of healthy subjects. The sample size must, of course, be increased to verify the found results.
Eventually, there could be a concern regarding a possible confounding factor. Although the subjects were instructed to show no verbal or nonverbal reaction to the exposed odors and the tester avoided to get into visual contact with the subject prior to and during the test an unconscious influence cannot ruled out completely. In this case the tester involuntary could have changed his or her profile of force application and therefore influenced the outcome. An unaware sudden start and steeper course of force rise would have favored an unstable behavior of the tested muscle. This is one reason why the slope before the breaking point was considered. The results invalidate the concern about unconscious manipulations by the tester because there is no relevant difference between the odors.
Characterization of “stable” and “unstable” adaptation
Taken the above-mentioned results together, it is suggested to define a “stable” and an “unstable” adaptation to an increasing external force as follows. A stable adaptation can be characterized by two conditions: (1) the AFisomax ≈ AFmax (≥ 98% of AFmax), thus, the muscle length stays quasi-isometric during the whole force rise (slight muscle suspensions are acceptable); (2) Oscillations of force with about 10 Hz arise during force increase, thus, AFosc is significantly lower than AFmax. Based on the data a percentage of averagely 76 ± 9% of AFosc to AFmax can be expected. An unstable adaptation is characterized by the following two conditions: (1) AFisomax is considerably lower than AFmax. Thus, the muscle lengthens during the force rise in submaximal areas and the maximum is reached under eccentric conditions (AFeccmax). Based on the data a percentage of 60 ± 10% of AFisomax to AFeccmax can be expected. (2) No or only poor oscillations on a high force level occur during the force rise, thus, AFosc is close to AFeccmax with a ratio of 94 ± 7%.
It is suggested that the unstable behavior reflects an inadequate adaptation of muscle length and tension to external increasing force applications. In the present study, this emerged by presenting a disgusting odor. This obviously is impairing the muscle function in the sense of AF in the here investigated small sample size of 10 healthy participants. For a first cautious summary thereof, a well-functioning undisturbed neuromuscular adaptation to an external force increase seems to be characterized by a sufficiently adapted muscle tension maintaining muscle length and limb position as well as by the occurrence of mechanical oscillations.
Neurophysiological explanation of muscular adaptations with regard to perception of olfactory inputs
Based on the own research, there are no comparable investigations concerning the behavior of AF – or other motor functions – as reaction to different odors. Trying to understand the underlying mechanisms, the suggestion of neuromuscular AF processing should be regarded more detailed. During the manual assessment of AF, the tested participant receives sensory inputs due to the tester’s contact and force application. Hereby, skin and joint receptors, muscle spindle cells and Golgi tendon organs are perceiving mechanical inputs. The sensory signals are forwarded through the posterior horn to other spinal and supraspinal structures42–44 and provide the current muscle length, tension and joint status. Sighting the literature, one can assume that at least the thalamus, cerebellum, inferior olivary nucleus (ION), red nucleus, basal ganglia, cingulate cortex and the sensorimotor cortex are involved in the complex processing of adaptive motor control and are interconnected directly or indirectly13–15,20,42–79. The cerebellum is considered as one of the most relevant sensorimotor structures concerning the temporal-spatial processing47,54. Its anterior part seems to be especially relevant for sensorimotor functions and the posterior part for cognition and emotions60. However, the posterior cerebellum also seems to be involved in the “prediction of sensory events”, especially for “timing perception and adjustment”54. Therefore, the cerebellum is relevant regarding the motoric adaptation15,61, whereby it seems to be of particular importance in the beginning of an adaptation61. As mentioned in the introduction, a mixed mechanism of feedback and feedforward control is assumed to be involved in the adaptive process15. The cerebellum seems to work as the forward controller in cooperation with the ION, which provides the motoric time signal45–48. Thereby, the cerebellum can learn to predict the accurate timing of connected events and, thereby, intervenes in motor control45,46,72. This flows into the error processing of motor control and provides the rhythmic neuronal signal to enable temporal coordinated movements45–47. The cerebellum receives information of the muscle spindle, Golgi tendon organs and skin receptors42. Therefore, it might be essential for the target-actual comparison of muscle length and tension. Reafferences are compared with a copy of the initial motoric command13. Mismatches are then corrected by adjustments of the motor output. It was suggested that the cerebellum is a kind of “error-correcting machine”, which compares the “expected and actual outcome of a sensory prediction or motor command”51. Also, other central structures seem to be relevant thereby. The parietal cortex was suggested as a central interface between sensory and motor processes concerning temporal processing71. Additionally, the thalamus is a central switching point for sensory and motor processes64, with its main task of modulating and regulating the flow of information to the cortex65. Meanwhile, the involvement of the cingulate cortex in emotions, pain processing as well as in spatial and motor control is secured14,20,57,68. This area reacts to different sensory inputs, e.g. exteroception, proprioception and nociception, and has a wide interconnection to other central structures20,57. Additionally, the basal ganglia work as a kind of filtration station for the muscle tone, including temporal processing, by facilitating desirable and inhibiting undesired motoric programs14,52,80. Last but not least the motor cortex receives information of the thalamus, the cerebellum, the basal ganglia, the red nucleus and of the limbic system54,58. The premotor cortex as well as the supplementary motor area of the cerebral cortex are involved in the temporal processing of motor activity71,73,81. Therefore, all those networked structures seem to be relevant in controlling the muscle length and tension during adaptation to external forces. Jörntell suggests, that “the final motor command, i.e. the final spatiotemporal structure of the activation of the α-motoneurons and thereby the muscles, is a sum or a product of all the motor command signals issued and the pattern of sensory feedback”53. As mentioned above, the occurred oscillations of 10 Hz during stable conditions (neutral/pleasant odors) might indicate a relevance of mechanical muscle oscillations in interaction with external forces. Those did not or only sparsely arise during unstable status (disgusting odor). Oscillations are also found in the mechanical38–41 as well as in electrical muscular activity76,82–86 during isometric muscle actions. They also occur in central structures during muscular activity. The cerebellum shows great inhibitory postsynaptic potentials of 8-17 Hz, which were found in cats50. Also other vertebrates exhibit oscillatory activity of the olivocerebellar circuitry of 10 Hz50,74. Additionally, the thalamus and neurons of the motor cortex are characterized by discharge frequencies between 11-30 Hz64 and 10 Hz87–89, respectively. Furthermore, the long latency reflexes of proprioception are processed with 10 Hz69,75. If an external force is changing, the corresponding correction also takes place with latencies of 10-12 Hz44,78. It is hypothesized that the found oscillations during the MMT could represent the normal functioning of the complex neuronal network standing behind it. With this prospect, their absence could possibly indicate irritations.
If the regulative circuitries are working properly, the adaptation in the sense of AF ought to be performed adequately (“stable”). The neuromuscular system should be able to adapt appropriately to the external force increase in time and space if the force increases not too abrupt or intense. However, the present study showed that this neuromuscular adaptation might be impaired by perceiving disgusting odor. Olfactory inputs are not transferred to the thalamus14. Initially, the cingulate cortex was reported to be associated with olfaction57. Olfactory afferences, with latencies of around 300ms90, are firstly transmitted to the olfactory bulb91 and then are projected directly to the piriform cortex and the limbic system (amygdala, hippocampus)91,92, which displays the close connection of olfaction and emotion33–35,93,94. Especially with perception of pleasant or disgusting odors, we assume the occurrence of positive or negative emotions, respectively. Therefore, it is likely that the here found reduced AFisomax and later occurred AFosc at a higher force level during perception of a disgusting odor might be related to a negative emotional component. A pilot-study investigating the AF under the influence of different emotions was performed and the results will be presented soon.
Characterization and specialty of the isometric Adaptive Force
The results strongly indicate that under particular circumstances a muscle can yield in length at a substantial submaximal force level. In this case the muscle loses its stability (ability to hold) despite of its further increase of tension. The maximum holding capacity (AFisomax) changes within a few seconds depending on the influence of odor. Therefore, in contrast to AFeccmax, AFisomax it seems to be sensitive regarding a disgusting olfactory influence, which is interpreted as a possible disturbing factor. The arising oscillations 10 Hz under stable conditions suggest this could not only be a characteristic for maintaining muscular stability but perhaps a prerequisite. A loss of this function could be a sign of a disturbed sensorimotor processing characterized by a muscle lengthening at a considerably low AF. It is suggested that the AFisomax, presumably depending on the onset of oscillations, seems to be the most vulnerable and, therefore, the possibly most relevant parameter in adapting to external forces. The immediate responses of AFisomax to the here investigated olfactory input strongly indicate to be based on regulatory mechanisms. Because of the close linkage of olfactory and emotional processing, the observed effect could possibly run via the influence of the limbic system on motor control95,96. However, the integration of the different central structures during adaptive motor processes leads to the conceivable and even likely assumption that also other internal and external inputs which enter the control circuitries might influence the adaptive motor control processes. The influence of health complaints on muscle function is reported for several indications, e.g. for infections as COVID-1997, post-infectious diseases98, CFS/ME99,100, cancer101, sarcopenia102,103, hormonal dysfunctions104,105 or fibromyalgia106. Thereby, possible nociception or other disturbing inputs might function as interferences in the complex motor control processes. We assume an impairment of the AFisomax thereby.
When a muscle gets unstable under certain circumstances this could lead to a destabilization of joints especially when they are under strain. A higher vulnerability regarding joint complaints or even injuries might arise in the process. In contrast to measure maximal forces as usual, the assessment of the special parameter AFisomax could provide a novel approach to understand injuries or orthopedic pathomechanisms.
Summarizing, the results highlight not only the suggested possibility of measuring a special adaptive neuromuscular control by the AF but might also deliver an approach for investigating the neuromuscular system regarding disturbances in the control circuits. The literature speaks for a complex control cascade as well as parallel working processes between the central areas characterized by oscillations which are involved in the control of the spatio-temporal structure of motor output. In an undisturbed, healthy neuromuscular system those complex control processes should enable the participant to adapt adequately to the external force stimuli.
In conclusion, the present study showed different adaptive motor outputs as a reaction to neutral, pleasant and disgusting odors in healthy persons. Assuming that the AF in reaction to neutral and pleasant odors reflect “normal” muscle function, the AF patterns during disgusting odor are interpreted as a disturbance of the neuromuscular control due to the unpleasant olfactory input. Based on the presented preliminary results, it is suggested that the length-tension control of muscles is affected thereby. Therefore, the isometric holding function including the peripheral mechanical muscle oscillations might be one or even the decisive parameter characterizing a well-functioning neuromuscular control of AF-action. It is hypothesized that measuring the AF, in particular the parameters AFisomax and AFosc, might be a suitable diagnostic tool to assess the functionality of neuromuscular control.
Based on the complex neuronal control, which is assumed to underlie the processing of AF, it is presumed that also other inputs as mental stress (negative emotions), nociception of joints or tissues or others might influence the AF as shown here for disgusting odors. If this hypothesis could be verified by further investigations, this might offer the possibility to use the measurement of AF as an individual diagnostic tool. The MMT is already used since decades36,37. However, due to the reasonable criticism of subjectivity, some skepticism concerning the AF tested by the MMT remains in different fields for which it might have potential. The acceptance could be improved by objectification using appropriate devices. The assessment and recording of the manually tested AF are necessary to secure a reliable and valid force profile of the tester. Because of the preliminary character of the present study further measurements with an enlarged data base are needed. In a next step, the AF in reaction to emotions and nociception should verify further evidence of the possible responses of the neuromuscular control to different inputs.