* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Research in Mammalian Mastication1
Brain–computer interface wikipedia , lookup
Neural engineering wikipedia , lookup
Neurocomputational speech processing wikipedia , lookup
Eyeblink conditioning wikipedia , lookup
Environmental enrichment wikipedia , lookup
Proprioception wikipedia , lookup
Metastability in the brain wikipedia , lookup
Synaptogenesis wikipedia , lookup
Neuroeconomics wikipedia , lookup
Neural oscillation wikipedia , lookup
Feature detection (nervous system) wikipedia , lookup
Microneurography wikipedia , lookup
Neuroplasticity wikipedia , lookup
Electromyography wikipedia , lookup
Caridoid escape reaction wikipedia , lookup
Synaptic gating wikipedia , lookup
Development of the nervous system wikipedia , lookup
Cognitive neuroscience of music wikipedia , lookup
Neuropsychopharmacology wikipedia , lookup
Optogenetics wikipedia , lookup
Neuromuscular junction wikipedia , lookup
Channelrhodopsin wikipedia , lookup
Embodied language processing wikipedia , lookup
Motor cortex wikipedia , lookup
AMER. ZOOL., 25:365-374 (1985) Research in Mammalian Mastication1 KENNETH E. BYRD 2 School of Physical Therapy, Texas Woman's University, Houston, Texas 77030 and Department of Physiology, University of Texas Health Science Center at Houston Dental Branch, Houston, Texas SYNOPSIS. Ongoing research efforts in mammalian mastication have defined several broad areas of mutual interest to workers in the discipline. They are (1) interrelationships between masticatory movements, (2) actions of the masticatory muscles, (3) comparisons between masticatory structures and functions, (4) developmental aspects, (5) comparisons between limbs and jaws, and (6) neurophysiologic considerations. The roles (potential and actual) of masticatory central pattern generators, cerebral "mastication areas," different neural mechanisms between mammalian taxa, neurophysiologic/morphologic interactions, and biochemical factors within the total milieu of mammalian mastication are discussed. INTRODUCTION Almost 20 years have elapsed since the beginning of detailed studies of mammalian mastication (Hiiemae, 1978). These studies have typically combined electromyographic (EMG) data from the muscles of mastication with patterns of mandibular movement during the act of chewing. The oral behaviors of several mammalian taxa during mastication have now been described using varied methodologies (Hiiemae, 1967; Hiiemae and Ardran, 1968; Crompton and Hiiemae, 1970; Hiiemae and Crompton, 1971; Kallen and Gans, 1972; DeVree and Gans, 1973; Herring and Scapino, 1973; Hiiemae and Kay, 1973; Weijs, 1973,1975; Gans and DeVree, 1974; Kay and Hiiemae, 1974; Luschei and Goodwin, 1974; McNamara, 1974; Weijs andDantuma, 1975; Crompton et al, 1977; DeVree, 1977, 1979; Gorniak, 1977; Byrd etal, 1978; Tal and Goldberg, 1978, 1981; Franks, 1979; Gorniak and Gans, 1980; Byrd, 1981; Byrd and Garthwaite, 1981; Fish and Mendel, 1982; Mendel and Fish, 1983; Thomas and Peyton, 1983). Despite these past and continuing studies, the amount of detailed masticatory EMG and mandibular movement data for the Mammalia is relatively very little. The purpose of the American Society of Zoologists symposium "Mammalian Mastication: An Overview" was to allow participants to appraise past and current research efforts in the general area of mammalian mastication and also to suggest areas for future research. The purpose of this article is to introduce and comment upon the areas of research interest as presented at the symposium. Hopefully, this article will "seduce and induce" the reader into reading the following contributions as well as providing an appreciation of current problems in the discipline of mammalian mastication. INTERRELATIONSHIPS BETWEEN MASTICATORY MOVEMENTS As documented in Dr. Karen Hiiemae's presentation,3 masticatory movements are not limited to only the mandible and temporomandibular joint (TMJ). Movements of the mandible during mastication may be viewed as the outcome of several additional "masticatory subsystems." The suprahyoid musculature, infrahyoid musculature, hyoid bone, and the tongue all play important roles in the masticatory act. Mastication can be denned as "mechanical digestion" of foodstuffs prior to 1 From the Symposium on Mammalian Mastication: "chemical digestion" which occurs in the An Overview presented at the Annual Meeting of the American Society of Zoologists, 27-30 December gastrointestinal tract (Hiiemae et al., 1978). Mastication can also be viewed as a phe1983, at Philadelphia, Pennsylvania. ! Present address: Department of Basic Sciences, School of Dentistry, University of Southern California, University Park—MC 0641, Los Angeles, California 90089-0641. * Dr. Hiiemae's paper was presented at the Philadelphia meeting, but is not included in this volume. 365 366 KENNETH E. BYRD nomenon largely resulting from the actions of the classically defined "muscles of mastication" (masseter, temporalis, lateral pterygoid, medial pterygoid, anterior digastric). On the other hand, movements of the hyoid and tongue are largely involved with intraoral food transport (Hiiemae et al., 1981). Normal mammalian feeding patterns use both intraoral food transport and mastication systems. As Dr. Hiiemae's article shows, both systems are synchronized and modulated by complex neural mechanisms. The role of the nervous system in effecting and affecting both these systems is probably more important than previous studies have imagined. ACTIONS OF THE MASTICATORY MUSCLES Dr. Gary Gorniak outlines the current knowledge base concerning the action of masticatory muscles within the Mammalia. As he asserts, despite studies drawn from most mammalian orders, the total range of diversity in form and function of the mammalian masticatory apparatus is still largely unknown. Traditional studies of the mammalian masticatory apparatus have concentrated upon morphological aspects of the skull, dentition, masticatory muscles, and vector analyses of mastication. These studies continue to be of great importance in the documentation of mammalian masticatory structures. Without such documentation, the physiological data are in limbo and unable to allow precise correlations between structure and function. Electromyography (EMG) and computerized data acquisition systems have allowed more efficient collection of masticatory movement and muscle activity data. Dr. Gorniak provides an overview of the different techniques used; each has its advantages and disadvantages, not to mention the inherent difficulties in comparing data obtained by different methodologies. Despite methodological dissimilarities between different studies, certain communalities emerge from the pooled mammalian masticatory studies. Certain muscles are associated with specific mandibular movements during mastication. These sim- ilarities provide an evolutionary "touchstone" by which researchers may yet determine phylogenetic relationships through careful comparison of mammalian masticatory patterns. COMPARISONS BETWEEN STRUCTURE AND FUNCTION The methodological and conceptual difficulties in making valid comparisons between mammalian masticatory structures and functions are discussed by Dr. Carl Gans. As Dr. Gans points out, a major difficulty in attempting any comparison is how one separates and then measures masticatory structure, function, and their development (ontogeny). The problem is made more difficult due to the mosaic nature of biologic systems: Different systems within an organism are now known to evolve at different rates (Cherry et al., 1978). The addition of homoplastic structures and functions further complicates the picture. Dr. Gans makes the point that masticatory functions are made up, in part, of "biological roles." These masticatory biological roles would be important recipients of any selective processes. In other words, structure subserves function in an evolutionary sense. A major concern for the evolutionary biologist is to precisely identify which part, or parts, of masticatory functions are actually biological roles. As Dr. Gans mentioned in his presentation in the symposium, the actual role of food items upon the mammalian masticatory apparatus is not to be neglected. Food item influences may be either long term (phylogenetic) or relatively short term (ontogenetic). Research in this area has been of prime interest to physical anthropologists in past and recent years (Molnar, 1972; Kay and Hiiemae, 1974; Hylander, 1975, 1977, 1979; Swindler and Sirianni, 1975; Kay, 1977a, b; Molnar and Gantt, 1977; Sheine and Kay, 1977; Walker et al., 1978; Beecher, 1979; Hinton and Carlson, 1979; Corruccini, 1980; Beecher and Corruccini, 1981; Fish and Mendel, 1982; Gordon, 1982; Molnar et al., 1983; Gordon, 1984). More data on nonprimate taxa need to be collected, however. RESEARCH IN MAMMALIAN MASTICATION DEVELOPMENTAL ASPECTS Dr. Sue Herring's contribution outlines the importance of ontogenetic factors in mammalian mastication. Analyses of the shift from suckling to chewing oral behaviors in most mammals (exceptions: precocious taxa like Cavia) may prove very useful in understanding the evolution of different masticatory specializations. In this sense, altricial mammals may serve as models for the study of development of mammalian mastication. Previous ideas concerning the shift from suckling to chewing oral behaviors have generally fallen into two camps: (1) that mastication gradually develops from a previously established suckling neuromuscular network (Dellow, 1969; Sessle, 1976), or (2) mastication arises de novo with development of completely separate neuromuscular elements associated with dental eruption (Bosma, 1967; Moyers, 1973). Dr. Herring presents new data on this problem. The possibility exists that developmental timing of masticatory muscles, nerves, and neurons is the critical factor in the ontogeny of mammalian mastication. Such differences in development sequencing may account for the suppression of those neural mechanisms responsible for suckling and their replacement by adult ingestive behaviors (Hall, 1979; Epstein, 1984). It would appear that ontogenetic changes in mastication and deglutition are part of the normal aging process in all mammals. Within aged humans, however, significant differences exist between males and females in terms of their respective oral behavior patterns (Baum and Bodner, 1983). Recently, the hypothesis that mammalian mastication develops from previously established suckling mechanisms received support from a nonmammalian source. In frogs, it has been documented that no new trigeminal motoneurons appear during larval maturation or metamorphosis (Alley and Barnes, 1983). In addition, there is a 90% retention of primary trigeminal motoneurons between larval and adult nervous systems (Barnes and Alley, 1983). The idea of "respecification" of trigeminal motoneurons to different peripheral targets was 367 proposed to explain these data (Alley and Barnes, 1983). A similar developmental mechanism may exist in mammals which could account for the neuromuscular shift between suckling and mastication. LIMBS AND JAWS Dr. Art English compares and contrasts data from mammalian jaw and limb muscles in his contribution. As he points out, mechanical models have been used to explain the diversity of both mammalian masticatory and locomotive specializations. Many of these studies, however, have not integrated available models or tested actual mechanisms of mammalian jaw and limb functions. Anatomical studies have suggested that jaw muscle fiber architecture exhibits "functional localization" while limb muscle fiber architecture suggests more uniformity in its functional manifestations. Muscle histochemistry, however, has demonstrated that within both jaw and limb muscles, there is considerable functional heterogeneity (Burke et al., 1973; Maxwell et al, 1973; Kugelberg, 1976; Maxwell et al, 1979; Clark and Luschei, 1981). These studies indicate that within individual jaw and limb muscles there is considerable heterogeneity of fiber types and distribution patterns; these fiber types and distribution patterns are also influenced by the age and sex of the individual (Maxwell et al, 1979). Related to muscular heterogeneity is the concept of neuromuscular compartments. As Dr. English explains, intramuscular motor units tend to operate in functionally distinct groups called neuromuscular compartments (NMC). Jaw and limb NMC appear similar in their basic architecture as indicated by preliminary data at this time. The anatomical presence of NMC is important because it implies that there are multiple, independent functional subdivisions within both jaw and limb muscles. NMC might account for the variability of intramuscular EMG data reported by individual researchers. NEUROPHYSIOLOGIC CONSIDERATIONS Much like muscular heterogeneity, neuromuscular compartments, ontogenetic 368 KENNETH E. BYRD sents the repository of distinct oral movement patterns (gnawing, unilateral chewing on right, unilateral chewing on left, suckling, etc.). It can be considered a hypothetical neural network that sets up a mechanical template for various oral movement patterns. The level B interneurons act as the pathway by which the distinct motor programs are provided to the program selector while the level A interneurons provide feedback to the motor programmer (Fig. 1). The oscillator/timer serves much like an "idle" or "internal drive" as defined by Tatton and Bruce (1981) and is responsible for the repetitive, Central pattern generators Central pattern generators (CPGs) rhythmic nature of the selected oral movelocated within the central nervous system ment pattern. The program selector is connected to and capable of generating rhythmic motor activities have been defined in many organ- the actual motor subroutines by the selecisms (Delcomyn, 1980). CPGs are capable tor interneurons (C in Fig. 1); these output of generating properly timed and some- neurons specify a series of motor subroutimes complex rhythmic movements in the tines necessary to complete a particular oral absence of peripheral nervous system feed- movement pattern. Motor subroutine neuback. A masticatory CPG can be defined rons code for specific mandibular moveas one which produces rhythmic alternat- ment patterns (elevate, depress, lateral ing activity in the motoneurons innervat- movement, medial movement, retrude, ing the closing and opening muscles of the protrude) while level A' and B' interneujaw (Luschei and Goldberg, 1981). The rons allow feedback between the motor complex nature of mandibular movement programmer and motor subroutines. Level and muscle activity patterns that occur 2 and 5a interneurons allow feedback during mammalian mastication strongly between the motor subroutines and the suggests that the masticatory CPG is more sensory processing network (thalamus, sensory cerebral cortex, cerebellum, etc.); than just a "neural oscillator." these interneurons provide the appropriate input to advance the program to the A new masticatory CPG model Figure 1 depicts a proposed hypothetical next subroutine. It should be noted that model for the mammalian masticatory the program selector determines the actual CPG. This model is modified from one order (sequence) in which each motor subprovided by Tatton and Bruce for loco- routine occurs, however. motor movements (1981). The model The level D interneurons, or command shown in Figure 1 assumes that the mas- interneurons of Kennedy (1969,1976), are ticatory CPG is located somewhere within the output neurons of the motor subrouthe pontine reticular formation and is tine "directory." Each level D interneuron therefore subcortical in nature. In this model would enable a single motor subroutine to (Fig. 1), the actual masticatory CPG is made be translated by the STST. The STST genup of functionally distinct groups of neu- erates both spatial and temporal comporons which comprise a motor programmer, nents of the motor program instructions program selector, oscillator/timer, motor that actually pattern motoneuron activity subroutines, and STST (spatial and tem- (Tatton and Bruce, 1981). In other words, poral sequence translator) together with STST neurons "decide" when it is behavtheir respective connecting interneurons. iorally appropriate to inhibit those motoThe motor programmer (Fig. 1) repre- neurons effecting certain undesired moveshifts, form/function interactions, and physiologic data, the neurophysiology of mastication is becoming more complex with continued research efforts. The reader is invited to read a recent review of masticatory neurophysiology research by Luschei and Goldberg (1981) in order to obtain an appreciation of previous research efforts and models of masticatory motor control. This section will concentrate upon some aspects of masticatory neurophysiologic research since Luschei and Goldberg's review article. 369 RESEARCH IN MAMMALIAN MASTICATION ments. The STST is equivalent to the switching and sequencing network of Tattonand Bruce (1981). Driver neurons (Kennedy, 1976) are concerned with nontemporal alteration of the selected oral movement pattern. For example, they would cause one chew cycle to become more narrow while the next cycle might be wider. Driver neurons are therefore directly connected and relay activity patterns to individual masticatory motoneurons. Level 3 interneurons between the sensory processing network and the driver neurons serve to modify the manifestation of specific subroutine instructions during their actual execution. The magnitude or "gain" of driver neuron signals are relayed to both the central sensory processing network and peripheral sensory afferents by level 5b interneurons. Individual motoneurons then effect individual muscle units within the muscles of mastication in whatever order specified by the CPG and a given oral movement pattern results. It should be noted that the sensory processing network interfaces with the motor programmer, program selector, and motor subroutine elements of the masticatory CPG (Fig. 1). Level 4 interneurons reaffirm the actual profile of the programmed movement to the motor programmer while level 1 interneurons initiate the proper motor program in response to the relevant portion of sensory input. Evidence for the proposed model Although a masticatory pattern generator has been suspected for almost 100 years (Ferrier, 1886; Rethi, 1893; Economo, 1902), the location of a masticatory CPG within the brainstem was not hypothesized until the 1920s-1930s (Bremer, 1923; Magoun et al, 1933; Rioch, 1934). Recent physiologic and anatomic research has provided additional data regarding the nature of the masticatory CPG as outlined in Luschei and Goldberg (1981) and described earlier here. Lund et al. (1983) have provided data which indicate that anterior digastric reflex amplitude and latency are cyclically modulated by the masticatory CPG and not by MOTOR PROGRAMMER ( Unilateral Cycles) OSCILLATOR TIMER MOTOR SUBROUTINES ( A a ) elevate mandible (Bb) move mandible medially ( C c ) depress mondible ( Dd) move mandible laterally ( E e ) move mandible anteriorly ( F f ) move mandible posteriorly SPATIAL and TEMPORAL SEQUENCE TRANSLATOR DRIVER NEURONS ( Nontemporal Alteration of Cycle; Alters Gain of Motor Subroutines) eg - make cycle narrow, wide, etc. FIG. 1. Hypothetical model for generation of mammalian masticatory patterns as modified from Tatton and Bruce (1981). The labeled arrows represent interneuronal pathways (either mono- or polysynaptic) between functional neuronal networks. Arrows labeled by letters (A-E) represent interneurons concerned with generation and execution of oral motor programs; number labeled arrows (l-5b) represent interneurons connecting sensory and motor networks. Motor subroutines (Aa-Ff) represent discrete mandibular movement patterns. The proposed system would effect unilateral chewing (as depicted here) by the program selector first selecting the unilateral cycle "template" from the motor programmer "repository" (arrows A and B). The program selector then specifies a series of motor subroutines by the selector interneurons (arrow C). For unilateral cycle mastication on the left, the hypothetical order of motor subroutine activation enabled by the spatial and temporal sequence translator (STST) would be (Cc Ff)(Cc Dd Ff)-(Aa Dd Ee)-(Aa Ee)-(Aa Bb Ee)-(Bb Cc Ee)-(Cc Ff). Therefore, in this model (Aa Bb Ee) and (Bb Cc Ee) respectively effect the buccal and lingual phases of power stroke; (Cc Ff) and (Cc Dd Ff) effect opening stroke; (Aa Dd Ee) and (Aa Ee) effect closing stroke. See text for additional detail. peripheral sensory feedback. They suggest that masticatory reflex circuits are cyclically modulated by either CNS interneurons or primary afferents. The existence 370 KENNETH E. BYRD of the STST postulated here is strength- damage to their respective trigeminal ened by data reported by Hellsing and motor nuclei demonstrates the importance Lindstrom (1983) which suggested that jaw of CPGs in the manifestation of mammaelevator synergists alternate or "rotate" lian patterns of mastication. their activity patterns during sustained isometric contractions in order to prevent Role of cerebral cortex muscular fatigue. Lesion studies of the sensorimotor corInjection of horseradish peroxidase tex in mammals suggest that the the cere(HRP) into the trigeminal motor nucleus bral cortex plays a role in the control of of cats has allowed recent identification of mastication (Luschei and Goldberg, 1981). premotor interneurons which connect with The cerebral cortex seems to be involved the trigeminal motor nucleus (Mizuno et in the voluntary modification of basic chew al., 1983). These interneurons are likely cycles manifested by the CPG. A "masticandidates for the driver neurons and level cation area" of the cerebral cortex has been 3 interneurons shown in Figure 1. Most of identified for several mammals and appears the HRP labeled interneurons were in the to be important in the voluntary control/ bilateral parvocellular reticular formation; modulation of mastication although not many were in the contralateral rostral- essential for the actual initiation of mastimost-cervical and caudalmost-medullary cation (Luschei and Goldberg, 1981). reticular formation (Mizuno et al., 1983). Recent research has provided evidence Some of these labeled interneurons were that the cerebral motor cortex, although determined to project to the ipsilateral not essential for mastication, allows the mesencephalic nucleus, contralateral tri- manifestation of the masticatory CPG to geminal sensory nucleus, contralateral tri- be modified in some manner (Chandler and geminal motor nucleus, and bilateral spinal Goldberg, 1982; Goldberg et al., 1982; trigeminal nucleus. Lund et al., 1982). In the guinea pig, the Siegel and Tomaszewski (1983) have cortical mastication area can activate both obtained single unit activity data from the (1) a polysynaptic pathway from cortex to medial reticular formation in unrestrained trigeminal motoneurons innervating mascats. They identified 6 cells, located within ticatory muscles, and (2) the brainstem the medial pontine and midbrain regions masticatory CPG (Chandler and Goldberg, of the reticular formation, that were most 1982). active during crushing of food pellets but Nozaki et al. (1983) have identified that were inactive during rhythmic chewing of portion of the reticular formation in cats ground meat and other soft foods. These involved with the pathway between ceredata further suggest that the masticatory bral motor cortex and trigeminal motoCPG is indeed located within the reticular neurons. HRP injection into the bulbar formation as do connections between the reticular formation revealed two types of ventral-medullary reticular formation and interneurons: inhibitory neurons projecttrigeminal motor nucleus in sheep (Jean et ing to masseter motoneurons and excitaal, 1983). tory neurons projecting to anterior digasElectrolytic lesioning of the trigeminal tric motoneurons. Intracellular recording motor nucleus in guinea pigs alters the revealed that these neurons were active manifestation of their masticatory CPG during stimulation of cortical mastication (Byrd, 1983, 1984). Despite their ability to areas and suggested that cortical control exhibit unilateral chew cycles, the lesioned of trigeminal motoneurons modulated by guinea pigs continued to produce the rel- these particular reticular formation interatively more complex bilateral chew cycles. neurons is separate from reflex control by Significant shifts in EMG activity durations peripheral inputs (Nozaki et al., 1983). occurred between working and balancing Ohta (1984) has recently stated that, in side muscles, however (Byrd, 1984). The rats, frontal cortex and central amygdaloid fact that the lesioned animals continued to nucleus have "convergent control" of produce complex bilateral chews after mandibular depression due to the contra- RESEARCH IN MAMMALIAN MASTICATION 371 lateral activation of jaw opening motoneurons and inhibition of jaw closing ones. Ohta points out, however, that the lateral amygdaloid nucleus is active during jaw closing in cats and rabbits. of morphologic alterations due to changed CPG manifestation is limited by both genetic (individual genome) and environmental (nutritional status, diet, etc.) factors. Different neural mechanisms between taxa Biochemical considerations Ultimately, the basis for all aspects of Ohta's paper illustrates an important fact to students of mammalian mastication: Sig- masticatory activity patterns is on the nificantly different neural mechanisms molecular or biochemical level. Microineffecting mastication can occur across jection of glutamic acid into the periformammalian taxa. For example, ablation of nical region of the hypothalamus in cats the cortical mastication areas in dogs and elicits jaw opening (Bandler, 1982). Masmonkeys revealed that dogs recovered ticatory activity of the gastropod Aplysia is much faster than their monkey counter- apparently modulated by a serotonergic parts (Frank, 1900). Rabbits can eventually neuron (Rosen et al., 1983). The role of recover from bilateral lesions of the cor- chemical neurotransmitters in control of tical mastication area (Bremer, 1923) while masticatory activity patterns has not yet guinea pigs cannot and are unable to feed been defined. themselves (Rioch, 1934; Byrd and LusDIRECTIONS FOR FUTURE RESEARCH chei, unpublished data). Conversely, rats recover from such bilateral ablations of the It is safe to say that not one area of cerebral cortex and can feed themselves research within the broad discipline of quite effectively (Castro, 1972). "mammalian mastication" has been Detailed maps of trigeminal motoneu- exhausted. Precise anatomical studies are rons specific for each masticatory muscle still needed for the majority of mammalian continue to be compiled for various mam- masticatory specializations. Accurate and malian taxa. Recent examples are Tal precise physiologic studies have only been (1980), Mizuno et al. (1981), Jacquin et al. accomplished for relatively few mamma(1983), and Kemplay and Cavanagh (1983). lian taxa as have masticatory muscle hisThese maps show significant differences tochemistry, ontogenetic, neurophysiobetween mammalian taxa not so much in logic, and functional morphology studies. the topographic distribution of motoneu- Additional data for the role of masticatory rons, but in the extent of motoneuron rep- CPGs in the determination of craniofacial resentation for each muscle (Tal, 1980). form and function need to be collected. These differences also suggest important Precise identification of the components neurophysiologic differences between taxa. within the brainstem reticular formation making up the masticatory CPG need to Interactions between CPGs and craniofacial be identified for mammalian taxa. The role morphology of neuromuscular compartments and the Significant morphologic changes of the functional heterogeneity of masticatory craniofacial complex caused by altered muscles in the determination of masticamanifestation of the masticatory CPG in tory activity patterns need to be correlated guinea pigs suggest that intra- and inter- with both neurophysiologic and morphospecific differences in craniofacial form may logic data. be due, in part, to different CPGs within A new and potentially very important the Mammalia (Byrd, 1983, 1984). Altered area for research is the area of biochemical manifestation of respiratory CPGs has also factors mentioned previously and illusproduced profound morphologic alter- trated by Bandler (1982) and Rosen et al. ations of the craniofacial skeleton in rhesus (1983). Just as the discovery of DNA had macaques (Miller, 1978; Miller et al., 1982; tremendous impact upon all facets of biolVargervik etal, 1984). In such studies, the ogy, future identification of biochemical assumption is made that the actual amount factors affecting the various components 372 KENNETH E. BYRD of mammalian mastication will also have great importance. Frog perspective on the morphological difference between humans and chimpanzees. Science 200:209-211. Clark, R. W. and E. S. Luschei. 1981. Histochemical REFERENCES characteristics of mandibular muscles of monkeys. Exper. Neurol. 74:654-672. Alley, K. E. and M. D. Barnes. 1983. Birth dates of trigeminal motoneurons and metamorphic reor- Corruccini, R. S. 1980. Size and positioning of the ganization of the jaw myoneural system in frogs. teeth and infratemporal fossa relative to taxoJ. Comp. Neurol. 218:395-405. nomic and dietary variation in primates. Acta Anat. 107:231-235. Bandler, R. 1982. Identification of neuronal cell bodies mediating components of biting attack behav- Crompton, A. W. and K. M. Hiiemae. 1970. Molar iour in the cat: Induction of jaw opening followocclusion and mandibular movements during ing microinjections of glutamate into occlusion in the American opossum, Didelphis hypothalamus. Brain Res. 245:192-197. marsupialis. J. Linn. Soc. (Zool.) 49:21-47. Barnes, M. D. and K. E. Alley. 1983. Maturation and Crompton, A. W., A. J. Thexton, P. Parker, and K. Hiiemae. 1977. The activity of the hyoid and recycling of trigeminal motoneurons in anuran jaw muscles during the chewing of soft food in larvae. J. Comp. Neurol. 218:406-414. the American opossum. In D. Gilmore and B. Baum, B. J. and L. Bodner. 1983. Aging and oral Robinson (eds.), The biology of marsupials, Vol. II, motor function: Evidence for altered perforpp. 287-305. Biology and environment. Macmillan, mance among older persons. J. Dent. Res. 62: London. 2-6. Beecher, R. M. 1979. Functional significance of the Delcomyn, F. 1980. Neural basis of rhythmic behavior in animals. Science 210:492-498. mandibular symphysis. J. Morph. 159:117-130. Beecher, R. M. and R. S. Corruccini. 1981. Effects Dellow, P. G. 1969. Control mechanisms of mastiof dietary consistency on craniofacial and occlusal cation. Ann. Austr. Coll. Dent. Surg. 2:81-95. development in the rat. Angle Orthodont. 51: DeVree, F. 1977. Mastication in guinea pigs, Cavia 61-69. porcellus. Amer. Zool. 17:886. Bosnia, J. F. 1967. Human infant oral function. In DeVree, F. 1979. Electromyography of the mastiJ. F. Bosma (ed.), Symposium on oral sensation and catory muscles in guinea pigs. Amer. Zool. 19: perception, pp. 98-110. Charles C Thomas, 1012. Springfield. DeVree, F. and C. Gans. 1973. Masticatory responses of pygmy goats (Capra hircus) to different foods. Bremer, F. 1923. Physiologie nerveuse de la mastiAmer. Zool. 13:1342-1343. cation chez le chat et le lapin. Arch. Int. Physiol. 21:308-352. Economo, C.J. 1902. Die centralen Bahnen des Kauund Schluckactes. Pflueg. Arch. Ges. Physiol. Burke, R. E., D. N. Levine, P. Tsairis, and F. E. Zajac. 1973. Physiological types and histochemical proMensch. Thiere 91:629-643. files in motor units of the cat gastrocnemius. J. Epstein, A. N. 1984. The ontogeny of neurochemical Physiol. 234:723-748. systems for control of feeding and drinking. Proc. Soc. Exper. Biol. Med. 175:127-134. Byrd, K. E. 1981. Mandibular movement and muscle activity during mastication in the guinea pig (Cavia Ferrier, D. 1886. The function of the brain. Putnam, porcellus). J. Morph. 170:147-169. New York. Byrd, K. E. 1983. Central pattern generators and Fish, D. R. and F. C. Mendel. 1982. Mandibular development of the mammalian craniofacial movement patterns relative to food types in comcomplex. Anat. Rec. 205:28A. mon tree shrews (Tupaia glis). Amer. J. Phys. Anthrop. 58:255-269. Byrd, K. E. 1984. Masticatory movements and EMG activity following electrolytic lesions of the tri- Frank, D. 1900. Uber die Beziehungen der Grosgeminal motor nucleus in growing guinea pigs. shirnrinde zum Vorgange der NahrungsaufAmer. J. Orthodont. 86:146-161. nahme. Arch. Anat. Physiol. Abt.:209-216. Byrd, K. E., D. J. Milberg, and E. S. Luschei. 1978. Franks, H. A. 1979. Analysis of rhythmic chewing Human and macaque mastication: A quantitative cycles in the hyrax. Amer. Zool. 19:1012. study. J. Dent. Res. 57:834-843. Gans, C. and F. DeVree. 1974. Correlation of accelerometers with electromyograph in the mastiByrd, K. E. and C. R. Garthwaite. 1981. Contour cation of pygmy goats (Capra hircus). Anat. Rec. analysis of masticatory jaw movements and mus178:360. cle activity in Macaca mulatta. Amer. J. Phys. Anthrop. 54:391-399. Goldberg, L. J., S. H. Chandler, and M. Tal. 1982. Relationship between jaw movements and triCastro, A. J. 1972. The effects of cortical ablations geminal motoneuron membrane-potential flucon digital usage in the rat. Brain Res. 37:173tuations during cortically induced rhythmical jaw 185. movements in the guinea pig. J. Neurophys. 48: Chandler, S. H. and L. J. Goldberg. 1982. Intracel110-125. lular analysis of synaptic mechanisms controlling spontaneous and cortically induced rhythmical Gordon, K. D. 1982. A study of microwear on chimjaw movements in the guinea pig. J. Neurophys. panzee molars: Implications for dental micro48:126-138. wear analysis. Amer. J. Phys. Anthrop. 59:195215. Cherry, L. M., S. M. Case, and A. C. Wilson. 1978. RESEARCH IN MAMMALIAN MASTICATION Gordon, K. D. 1984. The assessment of jaw movement direction from dental micro wear. Amer. J. Phys. Anthrop. 63:77-84. Gorniak, G. C. 1977. Feeding in golden hamsters, Mesocricetus auratus. J. Morph. 154:427-458. Gorniak, G. C. and C. Gans. 1980. Quantitative assay of electromyograms during mastication in domestic cats (Felis catus). J. Morph. 163:253281. Hall, W. G. 1979. The ontogeny of feeding in rats. J. Comp. Physiol. Psychol. 93:977-1000. Hellsing, G. and L. Lindstrom. 1983. Rotation of synergistic activity during isometric jaw closing muscle contraction in man. Acta Physiol. Scand. 118:203-207. Herring, S. W. and R. P. Scapino. 1973. Physiology of feeding in miniature pigs. J. Morph. 141:427— 460. Hiiemae, K. M. 1967. Masticatory function in the mammals. J. Dent. Res. 46:883-893. Hiiemae, K. M. 1978. Mammalian mastication: A review of the activity of the jaw muscles and the movements they produce in chewing. In P. M. Butler and K. A. Joysey (eds.), Development, func- 373 grade HRP study. J. Comp. Neurol. 218:239256. Jean, A., M. Amri, and A. Calas. 1983. Connections between the ventral medullary swallowing area and the trigeminal motor nucleus of the sheep studied by tracing techniques. J. Autonom. Nerv. Syst. 7:87-96. Kallen, F. C. and C. Gans. 1972. Mastication in the little brown bat (Myotis lucifugus).]. Morph. 136: 385-420. Kay, R. F. 1977a. Diets of early Miocene African hominoids. Nature 268:628-630. Kay, R. F. 19776. The evolution of molar occlusion in the Cercopithecidae and early catarrhines. Amer. J. Phys. Anthrop. 46:327-352. Kay, R. F. and K. M. Hiiemae. 1974. Jaw movement and tooth use in recent and fossil primates. Amer. J. Phys. Anthrop. 40:227-256. Kemplay, S. and J. B. Cavanagh. 1983. Bilateral innervation of the anterior digastric muscle by trigeminal motor neurons. J. Anat. 136:417-423. Kennedy, D. 1969. The control of output by central neurons. In M. A. B. Brazier (ed.), The interneuron, pp. 21-36. University of California Press, tion and evolution of teeth, pp. 359-398. Academic Berkeley. Press, London. Kennedy, D. 1976. Neuronal elements in relation to network function. In J. C. Fentress (ed.), Simpler Hiiemae, K. M. and G. M. Ardran. 1968. A cineranetworks and behavior, pp. 65—81. Sinauer, Masdiographic study of feeding in Rattus norvegicus. sachusetts. J. Zool. (London) 154:139-154. Hiiemae, K. M. and A. W. Crompton. 1971. A cine- Kugelberg, E. 1976. Adaptive transformation of rat fluorographic study of feeding in the American soleus motor units during growth. J. Neurol. Sci. opossum, Didelphis marsupialis. In A. A. Dahlberg 27:269-289. (ed.), Dental morphology and evolution, pp. 2 9 9 Lund, J. P., K. Appenteng, and J. J. Seguin. 1982. 334. University of Chicgo Press, Chicago. Analogies and common features in the speech and masticatory control systems. In S. Grillner, Hiiemae, K. M. and R. F. Kay. 1973. Evolutionary B. Lindblom, J. Lubker, and A. Persson (eds.), trends in the dynamics of primate mastication. In Speech motor control, pp. 231-245. Pergamon, M. R. Zingeser (ed.), Craniofacial biology of priOxford. mates, pp. 28-64. Karger, Basle. Hiiemae, K., A. J. Thexton, and A. W. Crompton. Lund, J. P., S. Enomoto, H. Hayashi, K. Hiraba, M. 1978. Intraoral food transport: The fundamenKatoh, Y. Nakamura, Y. Sahara, and M. Taira. 1983. Phase-linked variations in the amplitude tal mechanism of feeding. In D. S. Carlson and of the digastric nerve jaw-opening reflex response J. A. McNamara, Jr. (eds.), Muscle adaptation in the craniofacial region, pp. 181-208. Craniofacial during fictive mastication in the rabbit. Can. J. Growth Series Monog. No. 8, Ann Arbor. Physiol. Pharmacol. 61:1122-1128. Hiiemae, K., A. J. Thexton, J. D. McGarrick, and A. Luschei, E. S. and L. J. Goldberg. 1981. Neural W. Crompton. 1981. The movement of the cat mechanisms of mandibular control: Mastication hyoid during feeding. Arch. Oral Biol. 26:65and voluntary biting. In V. B. Brooks (ed.), Hand81. book of physiology—The nervous system, Vol. II, pp. 1237-1274. American Physiological Society, Hinton, R. J. and D. S. Carlson. 1979. Temporal Bethesda, Maryland. changes in human temporomandibular joint size and shape. Amer. J. Phys. Anthrop. 50:325-334. Luschei, E. S. and G. M. Goodwin. 1974. Patterns Hylander, W. L. 1975. Incisor size and diet in anthroof mandibular movement and jaw muscle activity poids with special reference to Cercopithecidae. during mastication in the monkey. J. Neurophys. Science 189:1095-1098. 37:954-966. Hylander, W. L. 1977. The adaptive significance of Magoun, H. W., S. W. Ranson, and C. Fisher. 1933. Corticofugal pathways for mastication, lapping, Eskimo craniofacial morphology. In A. A. Dahland other motor functions in the cat. Arch. Neuberg and T. M. Graber (eds.), Orofacialgrowth and rol. Psychiat. 30:292-308. development, pp. 129-169. Mouton, Paris. Hylander, W. L. 1979. The functional significance Maxwell, L. C , D. S. Carlson, J. A. McNamara, Jr., a n d j . A. Faulkner. 1979. Histochemical charofprimatemandibularform.J. Morph. 160:223240. acteristics of the masseter and temporalis muscles of the rhesus monkey (Macaca mulatto). Anat. Rec. Jacquin, M. F., R. W. Rhoades, H. L. Enfiejian, and 193:389-402. M. D. Egger. 1983. Organization and morphology of masticatory neurons in the rat: A retro- Maxwell, L. C , J. A. Faulkner, and D. A. Lieberman. 374 KENNETH E. BYRD 1973. Histochemical manifestations of age and endurance training in skeletal muscle fibers. Amer. J. Physiol. 344:356-361. McNamara, J. A., Jr. 1974. An electromyographic study of mastication in the rhesus monkey (Macaca mulatto}. Arch. Oral Biol. 19:821-823. Mendel, F. C. and D. R. Fish. 1983. Aspects of masticatory form/function in two-toed sloths, Choloepus hoffmanni. Anat. Rec. 205:129A. Miller, A. J. 1978. Electromyography of craniofacial musculature during oral respiration in the rhesus monkey {Macaca mulatto). Arch. Oral Biol. 23: 145-152. Miller, A. J., K. Vargervik, and G. Chierici. 1982. Sequential neuromuscular changes in rhesus monkeys during the initial adaptation to oral respiration. Amer. J. Orthodont. 81:99-107. Mizuno, N., K. Matsuda, N. Iwahori, M. UemuraSumi, M. Kume, and R. Matsushima. 1981. Representation of the masticatory muscles in the motor trigeminal nucleus of the macaque monkey. Neurosci. Letters 21:19-22. Mizuno, N., Y. Yasui, S. Nomura, K. Itoh, A. Konishi, M. Tanaka, and M. Kudo. 1983. A light and electron microscopic study of premotor neurons for the trigeminal motor nucleus. J. Comp. Neurol. 215:290-298. Molnar, S. 1972. Tooth wear and culture: A survey of tooth functions among some prehistoric populations. Curr. Anthrop. 13:511-526. Molnar, S. and D. G. Gantt. 1977. Functional implications of primate enamel thickness. Amer. J. Phys. Anthrop. 46:447-454. Molnar, S., J. K. McKee, I. M. Molnar, and T. R. Przybeck. 1983. Tooth wear rates among contemporary Australian aborigines. J. Dent. Res. 62:562-565. Moyers, R. E. 1973. Handbook of orthodontics. Year- book Medical, Chicago. Nozaki, S., S. Enomoto, and Y. Nakamura. 1983. Identification and input-output properties of bulbar reticular neurons involved in the cerebral cortical control of trigeminal motoneurons in cats. Exper. Brain Res. 49:363-372. Ohta, M. 1984. Amygdaloid and cortical facilitation or inhibition of trigeminal motoneurons in the rat. Brain Res. 291:39-48. Rethi, L. 1893. Das Rindenfeld, die subcorticalen Bahnen und das Coordinations-Centrum des Kauens und Schluckens. Akad. Wiss. Wien Math. Naturwiss. Kl. 102:359-377. Rioch, J. M. 1934. The neural mechanism of mastication. Amer. J. Physiol. 108:168-176. Rosen, S. C , I. Kupfermann, R. S. Goldstein, and K. R.Weiss. 1983. Lesions of a serotonergic mod- ulatory neuron in Aplysia produces a specific defect in feeding behavior. Brain Res. 260:151-155. Sessle, B.J. 1976. How are mastication and swallowing programmed and regulated? In B. J. Sessle and A. G. Hannam (eds.), Mastication and swallowing: Biological and clinical correlates, pp. 161 — 171. University of Toronto Press, Toronto. Sheine, W. S. and R. F. Kay. 1977. An analysis of chewed food particle size and its relationship to molar structure in the primates Cheirogaleus medius and Galago senegalensis and the insectivoran Tupaiaglis. Amer. J. Phys. Anthrop. 47:15-20. Siegel, J. M. and K. S. Tomaszewski. 1983. Behavioral organization of reticular formation: Studies in the unrestrained cat. I. Cells related to axial, limb, eye, and other movements. J. Neurophys. 50:696-716. Swindler, D. R. and J. E. Sirianni. 1975. Dental size and dietary habits of primates. Yearbook of Phys. Anthrop. 19:166-182. Tal, M. 1980. Representation of some masticatory muscles in the trigeminal motor nucleus of the guinea pig: Horseradish peroxidase study. Exper. Neurol. 70:726-730. Tal, M. and L.J.Goldberg. 1978. Masticatory muscle activity during rhythmic jaw movements in the anesthesized guinea pig. J. Dent. Res. 57A:130. Tal, M. and L.J.Goldberg. 1981. Masticatory muscle activity during rhythmic jaw movements in the anaesthetized guinea pig. Arch. Oral Biol. 26: 803-807. Tatton, W. G. and I. C. Bruce. 1981. Comment: A schema for the interactions between motor programs and sensory input. Can. J. Physiol. Pharmacol. 59:691-699. Thomas, N. R. and S. C. Peyton. 1983. An electromyographic study of mastication in the freelymoving rat. Arch. Oral Biol. 28:939-945. Vargervik, K., A. J. Miller, G. Chierici, E. Harvold, and B. S. Tomer. 1984. Morphologic response to changes in neuromuscular patterns experimentally induced by altered modes of respiration. Amer. J. Orhodont. 85:115-124. Walker, A., H. N. Hoeck, and L. Perez. 1978. Microwear of mammalian teeth as an indicator of diet. Science 201:908-910. Weijs, W. A. 1973. Functional morphology of the masticatory apparatus of the albino rat. Acta Morph. Need. Scand. 11:321-340. Weijs, W. A. 1975. Mandibular movements of the albino rat during feeding. J. Morph. 154:107124. Weijs, W. A. and R. Dantuma. 1975. Electromyography and mechanics of mastication in the albino rat.J. Morph. 146:1-34. SCIENCE AS A WAY OF KNOWING An Ongoing Project of the Education Committee of the American Society of Zoologists Cosponsored by The American Society of Naturalists The Society for the Study of Evolution The Biological Sciences Curriculum Study The American Institute of Biological Sciences The American Association for the Advancement of Science The Association for Biology Laboratory Education The National Association of Biology Teachers The Society for College Science Teachers The Ecological Society of America The Genetics Society of America and the University of California at Riverside II SCIENCE AS A WAY OF KNOWINGHUMAN ECOLOGY CONTENTS John A. Moore Science as a way of knowing—Human ecology. Opening remarks 377 Paul R. Ehrlich Human ecology for introductory biology courses: An overview 379 Anne H. Ehrlich The human population: Size and dynamics 395 John L. Fischer Science as a way of knowing: Man and food 407 James N. Pitts, Jr. On the trail of atmospheric mutagens and carcinogens: A combined chemical/microbiological approach . . . 415 Trends in health—Ecological consequences for the human Lester Breslow population 433 Robert M. May Ecological aspects of disease and human populations . . 441 G. Carleton Ray Man and the sea—The ecological challenge Garrett Hardin Human ecology: The subversive, conservative science . . 469 Gary Anderson and Films and videotapes in human ecology 477 Science as a way of knowing—Human ecology 483 Index 639 451 Nathan H. Hart John A. Moore