Whisking musculature

• Dr. Sebastian Haidarliu, Department of Neurobiology, The Weizmann Institute, Rehovot

Definition

Whisking musculature is represented by a group of facial striated muscles that have their insertion sites within the mystacial pad and control vibrissa movements in whisking mammals. The role of the vibrissa movements in active rats for equilibration, determining nearness or position of edges or corners, as well as discrimination of inequalities of surface as a compensation for a poor vision was described for the first time by Vincent (1912). The ability to move vibrissae rhythmically during tactile exploration of the environment (whisking) was then observed in many other rodents, such as mice, hamsters, gerbils, squirrels and porcupines (Welker, 1964; Woolsey et al., 1975; Rice et al., 1986; Munz et al., 2010), in insectivores, such as Etruscan shrew (Anjum et al., 2006) and greater hedgehog tenrec (Mitchinson et al., 2011), and in marsupials, such as Brazilian short-tailed and Virginia opossums (Rice et al., 1986; Mitchinson et al., 2011). The whisking musculature moves vibrissa-sinus complexes in such a way that vibrissae can scan the whole space around animal snout for precise detecting eventual objects. Whisking muscles move vibrissae with the aid of connective tissue (collagenous skeleton) and are the principal mover of the vibrissae in the “vibrissal motor plant” described by Hill et al. (2008).

Classification

Whisking musculature is represented by voluntary striated muscles. According to the location of the muscle origins, whisking muscles were grouped into two categories: intrinsic and extrinsic (Dörfl, 1982). Intrinsic muscles were first described by Vincent (1913) under the name of “follicle muscles”. They originate and insert within the mystacial pad. Extrinsic muscles originate outside, and insert within the mystacial pad. According to the direction in which extrinsic muscles move the vibrissae, they can be divided into three groups: protractors, retractors, and vertical vibrissa deflectors. Based on the shape and the orientation of the muscle fibers, whisking muscles can be attributed to parallel, convergent (fan-shaped), and pennate types.

Anatomy

Methodology

The first anatomical schemes of the whisking muscle arrangement within the mystacial pad were obtained by using methods of dissection. Using these methods, majority of whisking muscles, including their origins and insertion sites, were described (Huber, 1930a, b; Meinertz, 1944; Rinker, 1954; Klingener, 1964; Ryan, 1989). However, a detailed complete map of whisking muscle arrangement was obtained after visualizing muscle fibers in the slices of the mystacial pad in situ using histoenzymatic methods of muscle staining. By these methods, additional muscles, such as Pars interna profunda and pseudointrinsic slips of the Pars interna of the M. nasolabialis profundus, which were not observed by using traditional methods of dissection, were revealed (Haidarliu et al., 2010).

Intrinsic muscles

Intrinsic muscles connect adjacent vibrissa follicles within the rows of the mystacial pad. Each intrinsic muscle is represented by two extremities (dorsal and ventral). The extremities originate from the rostral surface of the proximal end of the rostrally located vibrissal follicle. Both extremities insert into the distal end of the neighboring, caudally located follicle, and into the contiguous corium. In mice and rats, intrinsic muscles connect adjacent vibrissal follicles only in the same row and look similar in all the vibrissal rows (Dörfl, 1982; Haidarliu et al., 2010, 2015) (Fig. 1). However, in some species, the arrangement of intrinsic muscles is different. For example, in big-clawed shrews, the arrangement of intrinsic muscles in the dorsal two rows (nasal compartment of the mystacial pad) is similar to that described in mice and rats, but in the ventral rows (maxillary compartment of the mystacial pad), their arrangement is hexagonal, and muscle extremities that originate from one follicle insert into two other caudally located follicles that belong to different rows (Yohro, 1977). In the marsupial Monodelphis domestica, in addition to regular intrinsic muscles within the two dorsal-most rows, there are additional oblique extremities that connect follicles within the rows A and B, and may cause rotational whisker movements (Grant et al., 2013). Intrinsic muscles of the most caudally located follicles (vibrissal arc that is composed of straddlers) insert into the corium caudal to the mystacial pad.

Figure 1: Light microscopy of a tangential slice of the mystacial pad of an adult mouse. Intrinsic muscles are revealed by staining for cytochrome oxidase activity and marked with arrow heads. (α − δ) Straddlers; (A1 – E1) first arc of the five vibrissal rows; (R) rostral; (V) ventral. Scale bar = 1 mm

Extrinsic muscles

Extrinsic muscles take their origin from the bones, cartilages or aponeuroses outside the mystacial pad, and insert into the corium or subcapsular fibrous mat within the mystacial pad. In mice and rats, extrinsic vibrissa protractors are represented by four subunits of the M. nasolabialis profundus: Partes media superior et inferior, and two subunits of the Pars interna. The first of them originates from the rostral end of the premaxilla, the second, from the intermuscular septum, and the last two, from the lateral wall of the nasal cartilage. All four extrinsic vibrissa protractors insert into the corium of the mystacial pad, and the last of them (pseudointrinsic) inserts also into the distal ends of the vibrissa follicles of the rows A and B (Haidarliu et al., 2010). Extrinsic vibrissa retractors are represented by two superficial and three deep muscles. Superficial extrinsic retractors (Mm. nasolabialis et maxillolabialis) are similarly represented also in other whisking species, such as hamsters (Wineski, 1985) and marsupials (Grant et al., 2013), originate from the skull, caudal to the mystacial pad, and are inserted into the corium of the mystacial pad between the rows of vibrissae (Fig. 2). Deep extrinsic retractors are represented by three parts of the M. nasolabialis profundus (Pars interna profunda, and Partes maxillares superficialis et profunda) that originate from the nasal cartilage and insert into the subcapsular fibrous mat (Fig. 3a). These muscles have a typical bipennate architecture (Fig. 3b) and were described also in hamsters (Wineski, 1985) and marsupials (Grant et al., 2013).

Figure 2: Light microscopy of a superficial tangential slice of the rat mystacial pad. Staining for cytochrome oxidase activity. (α − δ) Straddlers; (A - E) five rows of vibrissae; (N) nostril. (1) M. nasolabialis; (2) M. maxillolabialis; (3) Pars orbicularis oris of the M. buccinatorius. (R) Rostral; (V) ventral. Scale bar = 1 mm.

Figure 3: Light microscopy of a deep tangential slice (a) of the mouse mystacial pad. (b) Enlarged boxed area in (a). Staining for cytochrome oxidase activity. (1) Pars interna profunda; (2) and (3), Partes maxillares superficialis et profunda, respectively, of the M. nasolabialis profundus; (4) tendon; (5) muscle fibers. (R) Rostral; (V) ventral. Scale bars = 1 mm (a) and 0.1 mm (b).

Vertical vibrissa deflectors are represented by two muscles. One of them (M. transversus nasi) originates from the dorsal nasal aponeurosis and forms also myomyous origins along the midline (Fig. 4). It inserts into the corium of the nasal compartment of the mystacial pad. The other (Pars orbicularis oris of the M. buccinatorius) originates from the skin of the lower lip, and from the muscle bundles of the M. buccinatorius, and inserts into the corium of the maxillary compartment of the mystacial pad (Fig. 2). Extrinsic muscles of the mystacial pad and their attachment sites (entheses) are shown schematically in Figure 5 .

Figure 4: Light microscopy of a horizontal slice of the snout of a young rat. (1) M. transversus nasi. Scale bar = 1 mm.

Figure 5: Schematic drawing that represents arrangement of the extrinsic musculature of a rodent mystacial pad. (α − δ) Straddlers; A1 – E1, first arc of the vibrissal rows; 1 -5, 10 and 11 are subunits of the M. nasolabialis profundus: (1) Pars maxillaris profunda; (2) Pars maxillaris superficialis; (3) Posterior slips, and (4) Pseudointrinsic slips of the Pars interna; (5) Pars interna profunda; (10) Pars media inferior; (11) Pars media superior. (6) M. transversus nasi; (7) M. nasolabialis; (8) M. maxillolabialis; (9) Pars orbicularis oris of the M. buccinatorius. Encircled numbers designate extrinsic muscles that are inserted into the deep fibrous mat, the rest of muscles are inserted into the corium. Green numbers show extrinsic vibrissa protractors, red, vibrissa retractors, and blue numbers, vertical vibrissa deflectors.

Muscle Fiber Types

Striated muscles are composed of muscle fibers characterized by different metabolic properties that determine their functional abilities: speed of shortening, duration of high activity, fatigability. Based on the morphological and functional data, striated muscles were divided into red and white types that correspond to slow and fast muscles, respectively (McComas, 1996). When the typing is based on the muscle fiber staining, obtained results do not always agree (Staron, 1997; Scott et al., 2001). Using histochemical methods of staining for ATPase activity, three types of muscle fibers (red, white, and intermediate) were described in the diaphragm of different mammals (Padykula and Gauthier, 1963). After staining for cytochrome oxidase activity that addresses oxidative capacity of the muscle fibers, similar three fiber types were revealed randomly distributed in the M. nasolabialis of the rat mystacial pad (White and Vaughan, 1991) and in the Mm. nasolabialis and maxillolabialis in mice (Grant et al., 2014). Similar mosaic pattern of fiber type distribution was found in other extrinsic muscles of the rat mystacial pad (Fig. 6) (Haidarliu et al., 2010).

Figure 6: Muscle fiber types in a muscle fascicle of the Pars media inferior of the M. nasolabialis profundus in an adult rat. Staining for cytochrome oxidase activity. (i) Intermediate, (R) red, and (W) white muscle fibers. Scale bar = 0.1 mm.

Microscopic appearance of muscle fibers depends on the method that was used for their visualization so that attempts of muscle typing that are based on the comparison of images obtained using different methods can lead to confusing results (Edgerton and Simpson, 1969). In addition, metabolic profile and patterns of the distribution of muscle fibers may vary in different compartments of the same muscle (Katsura et al., 1982), can be altered by functional demands and aging (Guth and Yellin, 1971; Tomanek et al., 1973; Pette and Staron, 1997), and depend also on the body size of the animals (Gauthier and Padykula, 1966). The first typing of intrinsic muscle fibers was conducted by Yohro (1977) who stained snout serial slices of the big-clawed shrew with hematoxylin and eosin, and found that intrinsic muscles are composed of typical red fibers. When intrinsic muscles were typed by revealing reactivity of cytochrome oxidase, they were classified as containing mainly white fibers, with a few red and intermediate fibers observable along muscle extremities (Haidarliu et al., 2010). Immunohistochemical staining for myosin heavy chain types has shown that in both whisking (mice and rats) and non-whisking (guinea pigs) species, intrinsic muscles are composed predominantly of type 2B muscle fibers that provide fast vibrissa movements (Jin et al., 2004). Immunohistochemical method is one of the most precise methods in muscle typing, but extrinsic muscles of the mystacial pad were not yet satisfactory revealed by such analysis, and their typing is traditionally performed mostly according to their histochemical staining for ATPase or oxidative enzymes activities which reveal a mixture of various fiber types.

Muscle Fiber Organization

Muscle fiber arrangement within the muscles is one of the factors that contribute to muscle force and speed. Whisking muscles possess different patterns of their fiber arrangement relative to the axis of force generated by a muscle. Intrinsic muscles are characterized by parallel muscle fiber arrangement, with a curved segment at the rostral site of their attachment (muscle origin) to the follicles. Extrinsic vibrissa protractors (Partes mediae superior et inferior, and pseudointrinsic and posterior subunits of the Pars interna of the M. nasolabialis profundus), as well as superficial vibrissa retractors (Mm. nasolabialis et maxillolabialis), and ventral vibrissa deflector (Pars orbicularis oris of the M. buccinatorius) have a divergent (fan-shaped) fiber arrangement that permits to affect large areas of the corium in the entire mystacial pad or at least in one of its two compartments (Fig. 2). Deep vibrissa retractors (Partes maxillares superficialis et profunda, and Pars interna profunda) that pull rostrally the deep fibrous mat, together with the proximal ends of vibrissa follicles, have a leaf-shaped profile and bipennate fiber arrangement (Fig. 3). Physiological cross sectional area of these bipennate muscles exceeds their anatomical cross section area, that leads to a proportional increase of the total force during contraction (Gans, 1982), and simultaneous decrease of the velocity of contraction and of the target (insertion site) excursion (Lieber and Fridén, 2002). M. transversus nasi is composed of parallel muscle fibers that are inserted into the corium of the nasal compartment of the mystacial pad (Fig. 4).

Function

Whisking muscles are the principal providers of the vibrissal movements, and the distributors of the loads developed by their contraction in order to obtain a relevant whisking pattern. Vibrissa protraction is controlled by a combination of activity of intrinsic and extrinsic muscles, whereas retraction is brought about by extrinsic muscles and elastic forces of the mystacial pad (Hill et al., 2008). Intrinsic muscles can cause also vibrissa torsional rotation that may result from an asymmetric motor innervation of the two intrinsic muscle extremities (Dörfl, 1982; Knutsen et al., 2008), or, in addition, from the contraction of oblique intrinsic muscle extremities that were observed in marsupials (Grant et al., 2013). Extrinsic vibrissa protractors pull the corium of the mystacial pad rostrally together with the distal ends of vibrissae. They may also lead to a reduction of the rostrocaudal whisker field as well as of the vertical spread of the vibrissae that has been described during “foveal” whisking (Berg and Kleinfeld, 2003) and surface investigation by vibrissae (Grant et al., 2009, 2012). Superficial vibrissa retractors pull the corium of the mystacial pad caudally, together with the distal ends of vibrissae. Deep vibrissa retractors pull rostrally the subcapsular fibrous mat, together with the proximal ends of the vibrissa follicles in all whisking species, even if these muscles differ morphologically: in rodents, they run the full length of the pad (Wineski, 1985; Haidarliu et al., 2010, 2015), whereas in opossum, they are much shorter and actuate the pad via collagen bundles (Grant et al., 2013). Simultaneous contraction of the superficial and deep vibrissa retractors results in an enhanced retraction of the vibrissae of the entire mystacial pad. Additional contraction of the extrinsic vibrissa protractors may lead to a rostral translation of the entire mystacial pad. Each extrinsic muscle of the mystacial pad that moves vibrissae in the rostrocaudal direction, can be in synergistic or antagonistic relationships with other extrinsic muscles, and with intrinsic muscles. Dorsal vertical vibrissa deflector (M. transversus nasi) pulls the corium together with the distal ends of the follicles of the vibrissal rows A and B dorsomedially, while the ventral vibrissa deflector (Pars orbicularis oris of the M. buccinatorius) pulls the corium, together with the distal ends of the follicles of the vibrissal rows C – E, ventrocaudally. Contraction of these two muscles leads to an increase of the vertical vibrissal spread. Exploratory whisking in air is characterized by simple, rhythmic, synchronous and symmetric movements of the vibrissae of the both mystacial pads (Semba and Egger, 1986). If the vibrissae touch or actively palpate an object, their movements become complex and sophisticated (Brecht et al., 2006). Vibrissa movements can be asynchronous and asymmetric (Erzurumlu and Killackey 1979; Kleinfeld et al., 1999; Sachdev et al., 2002; Brecht et al., 2006; Ahissar and Knutsen, 2008; Deutsch et al., 2012; Sherman et al., 2013), with simultaneous torsional rotation (Knutsen et al., 2008; Grant et al., 2013). Such movements can be performed voluntarily or be triggered by head turning (Towal and Hartmann, 2006; Mitchinson et al., 2011).

Innervation

Mystacial pad is innervated by two cranial nerves: (i) the trigeminal nerve as a sensory nerve, and (ii) the facial nerve as a motor nerve controlling facial musculature. General scheme of the facial muscle innervation in different rodents is apparently similar, though there are interspecies differences in the distribution of small nerves and in their nomenclature. In mice, intrinsic muscles and ventral vibrissa retractor (M. maxillolabialis) receive motor innervation from the branches of the fused together rami buccolabiales superior et inferior of the facial nerve, whereas the dorsal vibrissa retractor (M. nasolabialis) receives branches from the ramus zygomatico-orbitalis after it fuses with the ramus temporalis of the facial nerve (Dörfl, 1985). In rats, vibrissal movements are controlled by the buccal branch and the upper division of the marginal mandibular branch of the facial nerve (Semba and Egger, 1986; Rice et al., 1993). In hamsters, rami buccolabiales superior et inferior of the facial nerve join together to form a buccal plexus at the anterior edge of the M. masseter and ventral margin of the M. maxillolabialis (Wineski, 1985). Buccal plexus innervates majority of facial striated muscles, and it was described in many other muroid rodents (Huber and Hughson, 1926; Rinker, 1954). There is also evidence that small hypoglossal neurons also project to the extrinsic musculature of the mystacial pad and compose a part of the hypoglossal-trigeminal loop that participates in sensory-motor control of the vibrissal system (Mameli et al., 2008).

Blood Supply

In rodents, external carotid artery is the main source of arterial supply to the face (Priddy and Brodie, 1948). It gives rise to external maxillary artery that passes in the rostral direction and gives branches to Pars orbicularis oris of the M. buccinatorius, then it turns dorsorostral and gives rise to its three terminal branches of which two are feeding the muscles of the mystacial pad: angular artery gives numerous branches to the Mm. nasolabialis et maxillolabialis, whereas superior labial artery passes rostrally and gives branches to the subunits of the M. nasolabialis profundus. Intrinsic muscles are supplied with blood from the arterioles that take their origin from the branches of the superior labial artery and pass within the core of mystacial pad giving rise to moderately dense networks of capillaries oriented longitudinally regarding fibers of each intrinsic muscle (Rice, 1993). These vessels receive predominantly peptidergic innervation, and during exploratory whisking behavior, they can meet enhanced metabolic demands of intrinsic muscles by increasing the overall blood flow (Fundin et al., 1997).

Development

The muscles of the head arise from somites that develop from the paraxial mesoderm, as well as from more rostral nonsomitic paraxial and prechordal head mesoderm (Kablar and Rudnicki, 2000). Two of these muscles (Mm. platysma myoides and sphincter colli) give rise to the muscles that control vibrissa movement (Huber, 1930a,b). Facial muscles that are associated with the rows A and B of vibrissae develop in the mouse embryos on the 12th developmental day, and can be revealed within the lateral nasal prominence, while those that are concerned with rows C – E, within the maxillary prominence (Yamakado and Yohro, 1979). Row-wise arrangement of the musculature related to the nasal and maxillary compartments of the mystacial pad suggests separate, though coordinated, development of both muscle groups within entire mystacial pad. Emergence of whisker movement is coming through two consecutive stages: twitching and whisking. Twitching was observed in sleeping newborn rats and was characterized by self-generated sleep-related twitches of single whiskers, as well as adjacent and non-adjacent whiskers, and complex movements comprising various subsets of whiskers moving in various directions (Tiriac et al., 2012). The movements dominate in the rostrocaudal direction, but are observed in other directions as well. The patterns of movements were consistent with the known anatomy of whisking musculature. Twitches correlated with the recorded electromyographic activity of the Mm. nasolabialis and maxillolabialis. Whisking emerges at the end of the second postnatal week (Welker, 1964; Landers and Zeigler, 2006; Grant et al., 2012) and may result from the maturation of the motor-sensory-motor loops (Saig et al., 2012).

Muscle-based Models of Whisking

For better understanding of the mechanisms of vibrissa movements, few attempts to create biomechanical models of the whisking musculature were undertaken. Hill et al. (2008) developed a biomechanical model of vibrissa motor plant and replicated the experimental observation that whisking results from three phases of extrinsic and intrinsic muscle activity. The model proposed by Simony et al. (2010) demonstrates direct translation from motoneuron spikes to vibrissa movements, and can serve as a building block in closed-loop motor-sensory models of active touch. Analysis of the model shows that contraction of a single intrinsic muscle results in movement of its two attached whiskers with different amplitudes; the relative amplitudes depend on the resting angles. Towal et al. (2011) quantified vibrissal array morphology and constructed a descriptive model of complete 3D morphology of the rat vibrissal array that was used to determine the constrains conditioned by muscle biomechanics. Combinations of these models can be used to simulate the contact patterns that would be generated as a rat uses its whiskers to tactually explore objects with varying curvatures.

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Sponsored by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Reviewed by: Anonymous (via Dr. David Golomb, Ben-Gurion University of the Negev, Be'er-Sheva, Israel)

Reviewed by: Prof. Ehud Ahissar, Department of Neurobiology, The Weizmann Institute, Rehovot

Reviewed by: Dr. Robyn Anne Grant, Conservation, Evolution and Behaviour Research Group, Manchester Metropolitan University, Manchester, UK

Accepted on: 2015-04-01 06:14:24 GMT