**3. Slow fluctuation of skull bone motion**

Data, which could be predict, that there are slow fluctuations of skull bone have been known more than a Century. However, the first direct observation concerned skull bone motion has been received by palpation of human skull [23], and it developed the special branch of medicine, - "Osteopathy", founded by Dr. A. Still, and actively spreading in USA since the end of XIX Century. This phenomenon consists in periodical with changeable amplitude and frequency skull bone movements, in range 6-12 cycles per minute. The high similarity of these fluctuations with respiratory movements was a reason to name these fluctuations as "Primary Respiratory Mechanism", or PRM. Decades of studies of PRM by palpation permits to describe peculiarities and consequences of involving of particular skull bone to motion, which are regular at normal conditions and different for pathology. During this time a number of conceptions and hypotheses of physiological nature of PRM have been formulated to explain the origin of these phenomena [24, 9]. Some of them were unreal from positions of biophysics and physiology, but at the present time there are acceptable conceptions which could be regarded as working hypothesis. From classical osteopathic positions, initial point of PRM is liquids disturbances in cranium, which slightly move the brain and acts to brain membrane in region of occipital and basis bone. This initiates movements of other skull bones.

One of the explanations of peculiarities PRM was based on reciprocal tension of brain membranes, which is popular up to the present time. However, brain membranes have no contractive elements and this is a current problem to accept of this conception, but skull membranes could play the role of passive "modulator" [25], which determine connection between movements of particular skull bones. Summary, the acceptable the conception, founded on the fact, that for cerebrovascular system is typical periodical changes of vascular tone. The consequent of these changes is intracranial pressure fluctuations, which may be a real physical force for deformation of skull pattern as united biomechanical system. Combination of fluctuations of intracranial pressure with additional role of skull membranes as passive modulator looks at the present time the most acceptable conception for slow periodical skull bone motions.

The experimental study of the skull bone motions started with cadaver observation, where skull bone motions were initiated by saline injection into the skull. These investigations give negative results. Later it was understood, that postmortem changes in sutures make skull as a solid body. Then instrumental investigations of living skull bone motion in animal experiments have been fulfilled [26, 27]. Human observation under physiological conditions on the base of modern technology, have been appeared at the end of XX Century. Firstly, direct observations demonstrated, that skull represents a complicated mechanical moveable system. This suggestion is based on investigations, represented device with needles inserted through cover skull tissues in human head and fixed in skull bone. Invisible movements of upper end of the needle were registered by means of small mirror fixed there, which are deflected laser beam, focused to the mirror [28].

70 Injury and Skeletal Biomechanics

fluid within the skull.

movements of other skull bones.

for slow periodical skull bone motions.

**3. Slow fluctuation of skull bone motion** 

It is important to emphasize that changes of the steady component of brain blood flow, determined by the perfusion pressure, are independent of the pulsatile component. The total brain blood supply is determined by the superposition of the steady state perfusion pressure (average level of arterial pressure) and the components of blood flow, which are in turn determined by the biomechanical properties of the skull and the mobility of cerebrospinal

Data, which could be predict, that there are slow fluctuations of skull bone have been known more than a Century. However, the first direct observation concerned skull bone motion has been received by palpation of human skull [23], and it developed the special branch of medicine, - "Osteopathy", founded by Dr. A. Still, and actively spreading in USA since the end of XIX Century. This phenomenon consists in periodical with changeable amplitude and frequency skull bone movements, in range 6-12 cycles per minute. The high similarity of these fluctuations with respiratory movements was a reason to name these fluctuations as "Primary Respiratory Mechanism", or PRM. Decades of studies of PRM by palpation permits to describe peculiarities and consequences of involving of particular skull bone to motion, which are regular at normal conditions and different for pathology. During this time a number of conceptions and hypotheses of physiological nature of PRM have been formulated to explain the origin of these phenomena [24, 9]. Some of them were unreal from positions of biophysics and physiology, but at the present time there are acceptable conceptions which could be regarded as working hypothesis. From classical osteopathic positions, initial point of PRM is liquids disturbances in cranium, which slightly move the brain and acts to brain membrane in region of occipital and basis bone. This initiates

One of the explanations of peculiarities PRM was based on reciprocal tension of brain membranes, which is popular up to the present time. However, brain membranes have no contractive elements and this is a current problem to accept of this conception, but skull membranes could play the role of passive "modulator" [25], which determine connection between movements of particular skull bones. Summary, the acceptable the conception, founded on the fact, that for cerebrovascular system is typical periodical changes of vascular tone. The consequent of these changes is intracranial pressure fluctuations, which may be a real physical force for deformation of skull pattern as united biomechanical system. Combination of fluctuations of intracranial pressure with additional role of skull membranes as passive modulator looks at the present time the most acceptable conception

The experimental study of the skull bone motions started with cadaver observation, where skull bone motions were initiated by saline injection into the skull. These investigations give negative results. Later it was understood, that postmortem changes in sutures make skull as a solid body. Then instrumental investigations of living skull bone motion in animal experiments have been fulfilled [26, 27]. Human observation under physiological conditions

**Figure 5.** Principle of transforming individual regions of image series into the amplitude-time plot: (a) input of the image series into a computer and specification of the analyzed region; (b) collocation of images and creation of the intermediate image; and (c) transformation of the intermediate image into the amplitude-time plot.

### 72 Injury and Skeletal Biomechanics

Approximately at the same time investigations, based on skull bone image analysis have been provided, using method of image computer analysis of serial MRI or X-Ray pictures – 30-45 single shots. Serial images of the skull were recorded by means of the Siemens-PolyStar angiographic system in 23 patients Principle of this method have been based on inserting to computer memory a number of equal fragments of skull bone image and, after an increase of their contrast superposition, small deviations of position of these fragments in united skull it is possibly as time dependent graph.(Fig. 5) These passive observation have shown, that, for normal physiological conditions, movements of skull fragment images, selected at of both MRI and X-Ray pictures, are periodical with irregular amplitude, fluctuating in ranges about 0.1-0.4 mm and frequency 5-12 cycles per minute (Fig.3 and Fig.6a).

The Role of Skull Mechanics in Mechanism of Cerebral Circulation 73

**Figure 6.** Fig.6 Cranial bone movements obtained by serial X-ray imaging (a) in a physiological state and (b) in the case of injection of radiopaque solution. The analyzed sections are shown in the center. (A) Consecutive image series showing changes in section shadows in the specified regions of cranial bones. (B) Changes in cranial bone positions in the specified sections shown in the amplitude-time plot. In all curves, the starting points of the time count are brought into coincidence and the time scale is the

(b)

(a)

same.

However, skull bone motion should be recorded it in conditions, closely to real physiological experiment, when skull bone motions are evoked by some external procedure, which may be fixed by intensity of intervention and its duration. Such conditions could be provided by observation of skull bone movements during angiographic procedure, taking for analysis cases with absence of clear pathology in cerebrovascular tree. During angiographic procedure, when into the skull through Internal Carotid Artery 20 ml of X-Ray contrast solution during one sec. is injected with pressure significantly higher than arterial pressure. During such procedure, about 15-18 X-Ray shots were made, which permits to evaluate by image analysis of skull bone motions with amplitude up to 0.7-0.9 mm, at the end of the phase of increasing of intracranial volume evoked by injection of solution, and decrease after 2.5-3.0 sec, when X-Ray solution has passed through brain vascular tree, and intracranial volume normalized (Fig.6 ). Taking into account, that average volume of intracranial cavity is about 1200ml, its increase on peak of X-Ray solution injection will be 1.0-1.5%. Taking this value into account it is possibly to suggest, that slow skull bone articular periodic fluctuations, accepted firstly manually and later instrumentally*,* represent about 0.2 – 0.4% of intracranial volume. At the present time stages of these skull motions are described in details [29, 30]. The fact, that skull bone movements are reciprocal, have been confirmed by simultaneous recording of REG with "lobe-occipital"(REG1) and "bitemporal"(REG2) position of electrodes. How it follows from Fig 6 Graph, with REG1-REG2 coordinates, that received two-dimensional pictures rather wide, which may be if comparative distance between electrodes is changed. That means, that every couple of electrodes moves reciprocally (Fig.7)

Thus, at the present time is confirmed, than slow skull bone motion are taking place and their motions are reciprocal. Similar slow fluctuations involve spinal cavity, too. In PRM phase of increasing volume of skull initiate to replacement of some volume of CSF to spinal cavity, which is possible, because volume-pressure changes are slow enough and CSF returned to the skull, when intracranial pressure decrease. The fact which confirmed this statement, have been received in experiments with animals [31] and demonstrated reciprocal slow volume changes in the skull and spinal cavity. Similar observations in humans have been received recently [21].

72 Injury and Skeletal Biomechanics

electrodes moves reciprocally (Fig.7)

humans have been received recently [21].

Fig.6a).

Approximately at the same time investigations, based on skull bone image analysis have been provided, using method of image computer analysis of serial MRI or X-Ray pictures – 30-45 single shots. Serial images of the skull were recorded by means of the Siemens-PolyStar angiographic system in 23 patients Principle of this method have been based on inserting to computer memory a number of equal fragments of skull bone image and, after an increase of their contrast superposition, small deviations of position of these fragments in united skull it is possibly as time dependent graph.(Fig. 5) These passive observation have shown, that, for normal physiological conditions, movements of skull fragment images, selected at of both MRI and X-Ray pictures, are periodical with irregular amplitude, fluctuating in ranges about 0.1-0.4 mm and frequency 5-12 cycles per minute (Fig.3 and

However, skull bone motion should be recorded it in conditions, closely to real physiological experiment, when skull bone motions are evoked by some external procedure, which may be fixed by intensity of intervention and its duration. Such conditions could be provided by observation of skull bone movements during angiographic procedure, taking for analysis cases with absence of clear pathology in cerebrovascular tree. During angiographic procedure, when into the skull through Internal Carotid Artery 20 ml of X-Ray contrast solution during one sec. is injected with pressure significantly higher than arterial pressure. During such procedure, about 15-18 X-Ray shots were made, which permits to evaluate by image analysis of skull bone motions with amplitude up to 0.7-0.9 mm, at the end of the phase of increasing of intracranial volume evoked by injection of solution, and decrease after 2.5-3.0 sec, when X-Ray solution has passed through brain vascular tree, and intracranial volume normalized (Fig.6 ). Taking into account, that average volume of intracranial cavity is about 1200ml, its increase on peak of X-Ray solution injection will be 1.0-1.5%. Taking this value into account it is possibly to suggest, that slow skull bone articular periodic fluctuations, accepted firstly manually and later instrumentally*,* represent about 0.2 – 0.4% of intracranial volume. At the present time stages of these skull motions are described in details [29, 30]. The fact, that skull bone movements are reciprocal, have been confirmed by simultaneous recording of REG with "lobe-occipital"(REG1) and "bitemporal"(REG2) position of electrodes. How it follows from Fig 6 Graph, with REG1-REG2 coordinates, that received two-dimensional pictures rather wide, which may be if comparative distance between electrodes is changed. That means, that every couple of

Thus, at the present time is confirmed, than slow skull bone motion are taking place and their motions are reciprocal. Similar slow fluctuations involve spinal cavity, too. In PRM phase of increasing volume of skull initiate to replacement of some volume of CSF to spinal cavity, which is possible, because volume-pressure changes are slow enough and CSF returned to the skull, when intracranial pressure decrease. The fact which confirmed this statement, have been received in experiments with animals [31] and demonstrated reciprocal slow volume changes in the skull and spinal cavity. Similar observations in

The Role of Skull Mechanics in Mechanism of Cerebral Circulation 73

**Figure 6.** Fig.6 Cranial bone movements obtained by serial X-ray imaging (a) in a physiological state and (b) in the case of injection of radiopaque solution. The analyzed sections are shown in the center. (A) Consecutive image series showing changes in section shadows in the specified regions of cranial bones. (B) Changes in cranial bone positions in the specified sections shown in the amplitude-time plot. In all curves, the starting points of the time count are brought into coincidence and the time scale is the same.

Mechanism of slow skull bone fluctuations is complicated and its study needs to establish why intracranial pressure is fluctuating. A real force for this may be activity of contractive structure inside the skull. Between different tissues and structures, filled cranial cavity, only one is capable of active change its mechanical properties due to external source of energy – that is smooth muscles of brain blood vessels. Because two facts – the presence of slow intracranial fluctuations and the presence only one contractive element inside cranial cavity – blood vessels wall smooth musculature, are confirmed, it is necessary to find possible linkage between two these processes.

The Role of Skull Mechanics in Mechanism of Cerebral Circulation 75

REG changes during this peak are one more confirmation of the skull pulse expanding. The second peak is corresponds to respiratory movement of chest. One more peak – low frequency corresponds to similar fluctuations, recorded by TCD and corresponds to slow fluctuation of central arterial pressure – Traube-Hering-Mayer waves. Between this peak and peaks, reflect chest respiratory movements, only on REG spectrum it is possible to see some one – three peaks, which didn't correspond to any peaks of respiratory and TCD records and belong to REG only. This is permits to think, that these peaks represent the origin of slow intracranial volume fluctuations, which corresponds to slow cranial bone motions, named as PRM. Generally, mechanism of slow fluctuation it is possible to present as scheme shown on Fig.9, which demonstrate, that very small, below one geometric degree comparative fluctuations of skull bone position could significantly change internal volume of cranial cavity and source of forces for these changes are fluctuations of intracranial pressure of different

The next and perhaps the last question in analyzed chain is the origin of slow cerebrovascular fluctuations, depended mainly on vascular tone. It is not yet definite answer to this question. However, it looks real prediction, that the fluctuations reflect control processes in the cerebrovascular system, because to vascular wall continuously acts different factors, everyone of which could change vascular tone. This is, first of all, different kinds of innervation – adrenergic, cholinergic, peptidergic and purinoergic nature [33], different mediators, nonorganic ions, autocoids, change of intravascular pressure and others [34]. Simultaneous, under normal living conditions, acting to vascular wall of numerous factors is the most real reason of appearing of some non-regular fluctuating process, which could be

reason of intracranial pressure fluctuating, evoked periodical skull bone movements.

The second is the data of REG, taken from sacral region of vertebral column.

rhythms, observation of which is "classical" method of osteopathy [35].

However, it is not only one reason for slow changes of intracranial pressure fluctuations, which may have connection with skull bone fluctuation. One of cranial osteopathy positions describes the special phenomenon, called crania-sacral rhythm. This is means the reciprocal movements of sacral section of vertebral column and the skull. Explanation of this phenomenon, given by osteopathy is not acceptable from point of view of biomechanics. Recently a new explanation, based on two facts has been appeared. One of these facts follows from MRI observation of pulse CSF movements in sagittal section of skull and neck.

If compare images, which have taken every 0.1s, it is possible to see that some portion of pulse CSF volume don't return to the skull and moves along to vertebral cord to its lumbar sack. REG records show, that cranial and sacral pulsations have reverse phases and level of REG gradually change. These data permit to formulate hypothesis, that during every pulse cycle some amount of CSF fills lumbar sack and pressure increased. Because hydrostatic forces are strong, this increase of lumbar sack could slightly erect sacral region of vertebral column, which is possible to feel by palpation. The erection may stimulate around sacral section muscles, which return it to initial position and CSF is returning back to cranium. This is, may be not perfect but some, basing on observation explanation of crania-sacral

origin, mainly due to vascular tone fluctuations.

**Figure 7.** Diagram of the experiment which demonstrates reciprocal skull bone motions. The 2-min recordings of REG by "cross" electrode position are represented on two-demention diagram (dark violet). This gives an ellipse due to REG fluctuations superposition. The axes of the ellipse reflect pulse and respiratory waves (long axe a-a) and reciprocal skull bone movements (short axe b-b).

From the side of cerebrovascular system, the fact of its slow periodic contraction, which are reason for similar changes of intracranial pressure, have been established in the first part of XX Century [7]. Later, it was shown, that brain blood volume, recorded by REG method and oxygen availability in brain tissue periodically changes in low frequency band [32]. It was establish, that oxygen availability fluctuations are very local and reflect, perhaps, in nervous tissue metabolic processes, but REG fluctuations reflect comparative wide brain region and show changes of brain blood volume. With purpose to find the correlation between this and other slow fluctuations, which are special for intracranial media, simultaneous recordings of REG in both hemispheres, TCD and chest movements were provided at a group of healthy persons 20-30 Years. It has been shown, that spectrum of all these processes is characterized by three kind of fluctuations (Fig 8). The first, the most pronounced peak is heart pulsation. REG changes during this peak are one more confirmation of the skull pulse expanding. The second peak is corresponds to respiratory movement of chest. One more peak – low frequency corresponds to similar fluctuations, recorded by TCD and corresponds to slow fluctuation of central arterial pressure – Traube-Hering-Mayer waves. Between this peak and peaks, reflect chest respiratory movements, only on REG spectrum it is possible to see some one – three peaks, which didn't correspond to any peaks of respiratory and TCD records and belong to REG only. This is permits to think, that these peaks represent the origin of slow intracranial volume fluctuations, which corresponds to slow cranial bone motions, named as PRM. Generally, mechanism of slow fluctuation it is possible to present as scheme shown on Fig.9, which demonstrate, that very small, below one geometric degree comparative fluctuations of skull bone position could significantly change internal volume of cranial cavity and source of forces for these changes are fluctuations of intracranial pressure of different origin, mainly due to vascular tone fluctuations.

74 Injury and Skeletal Biomechanics

linkage between two these processes.

Mechanism of slow skull bone fluctuations is complicated and its study needs to establish why intracranial pressure is fluctuating. A real force for this may be activity of contractive structure inside the skull. Between different tissues and structures, filled cranial cavity, only one is capable of active change its mechanical properties due to external source of energy – that is smooth muscles of brain blood vessels. Because two facts – the presence of slow intracranial fluctuations and the presence only one contractive element inside cranial cavity – blood vessels wall smooth musculature, are confirmed, it is necessary to find possible

**Figure 7.** Diagram of the experiment which demonstrates reciprocal skull bone motions. The 2-min recordings of REG by "cross" electrode position are represented on two-demention diagram (dark violet). This gives an ellipse due to REG fluctuations superposition. The axes of the ellipse reflect pulse

From the side of cerebrovascular system, the fact of its slow periodic contraction, which are reason for similar changes of intracranial pressure, have been established in the first part of XX Century [7]. Later, it was shown, that brain blood volume, recorded by REG method and oxygen availability in brain tissue periodically changes in low frequency band [32]. It was establish, that oxygen availability fluctuations are very local and reflect, perhaps, in nervous tissue metabolic processes, but REG fluctuations reflect comparative wide brain region and show changes of brain blood volume. With purpose to find the correlation between this and other slow fluctuations, which are special for intracranial media, simultaneous recordings of REG in both hemispheres, TCD and chest movements were provided at a group of healthy persons 20-30 Years. It has been shown, that spectrum of all these processes is characterized by three kind of fluctuations (Fig 8). The first, the most pronounced peak is heart pulsation.

and respiratory waves (long axe a-a) and reciprocal skull bone movements (short axe b-b).

The next and perhaps the last question in analyzed chain is the origin of slow cerebrovascular fluctuations, depended mainly on vascular tone. It is not yet definite answer to this question. However, it looks real prediction, that the fluctuations reflect control processes in the cerebrovascular system, because to vascular wall continuously acts different factors, everyone of which could change vascular tone. This is, first of all, different kinds of innervation – adrenergic, cholinergic, peptidergic and purinoergic nature [33], different mediators, nonorganic ions, autocoids, change of intravascular pressure and others [34]. Simultaneous, under normal living conditions, acting to vascular wall of numerous factors is the most real reason of appearing of some non-regular fluctuating process, which could be reason of intracranial pressure fluctuating, evoked periodical skull bone movements.

However, it is not only one reason for slow changes of intracranial pressure fluctuations, which may have connection with skull bone fluctuation. One of cranial osteopathy positions describes the special phenomenon, called crania-sacral rhythm. This is means the reciprocal movements of sacral section of vertebral column and the skull. Explanation of this phenomenon, given by osteopathy is not acceptable from point of view of biomechanics. Recently a new explanation, based on two facts has been appeared. One of these facts follows from MRI observation of pulse CSF movements in sagittal section of skull and neck. The second is the data of REG, taken from sacral region of vertebral column.

If compare images, which have taken every 0.1s, it is possible to see that some portion of pulse CSF volume don't return to the skull and moves along to vertebral cord to its lumbar sack. REG records show, that cranial and sacral pulsations have reverse phases and level of REG gradually change. These data permit to formulate hypothesis, that during every pulse cycle some amount of CSF fills lumbar sack and pressure increased. Because hydrostatic forces are strong, this increase of lumbar sack could slightly erect sacral region of vertebral column, which is possible to feel by palpation. The erection may stimulate around sacral section muscles, which return it to initial position and CSF is returning back to cranium. This is, may be not perfect but some, basing on observation explanation of crania-sacral rhythms, observation of which is "classical" method of osteopathy [35].

The Role of Skull Mechanics in Mechanism of Cerebral Circulation 77

**Figure 9.** Schematic representation of skull move motion, iniciated intracranial pressure , roun indicate

All above presented data show, that skull, its brain part is a moveable system. For the skull bone two kinds of movement are special. The first is rapid, during 0.1-0.15s skull expanding by pulse increased arterial pressure. This is too short time to involve CSF to balance intracranial blood volume and increase of volume of arteries mainly on skull basement increase pressure into the skull, which causes deforming its pattern by articular movements of bones in sutures which totally increase internal volume of skull by not much value – about 0.2-0.3% to compare with total volume cranial cavity. However, it is enough to accept additional 3-6 ml of blood, which are extremely important for maintain circulatorymetabolic supply of brain functioning. If this kind of skull mobility diminishes by some reason, brain circulatory insufficiently could appear, which may be reason of some such pathology situation, as brain dementia of circulatory origin. That is why on early steps of

Other kind of the skull bone movements is based on slow fluctuation of skull bone position, evoked by internal forces, finally expressed as periodical changes of intracranial pressure, which include processes in vertebral cord also. Actually, cranio-spinal space is represented

physiological origin (BROW) but may be pathological origin – (BLUE).

civilization, skull trepanation served as method of treatment.

**4. Conclusion** 

**Figure 8.** Spectral representation of healthy person, age 23, slow in range 0-1,6 Hz and range 0.04 Hz of REG, TCD and Respiration. Arrow (RED) show off central arterial pressure, Arrow Green – fluctuations of intracranial origin and BUE arrow show component of chest respiratory movements.

**Figure 9.** Schematic representation of skull move motion, iniciated intracranial pressure , roun indicate physiological origin (BROW) but may be pathological origin – (BLUE).
