Effects of aging on behavior and leg kinematics during locomotion in two species of cockroach

SUMMARY Aging is often associated with locomotor deficits. Behavior in aged Blaberus discoidalis cockroaches was analyzed during horizontal walking, climbing, righting and inclined walking. Adult animals showed a decrease in spontaneous locomotion with increasing age. Tarsal abnormalities, termed `tarsus catch', were often present in aged individuals. In `tarsus catch', the prothoracic leg catches on the mesothoracic leg during the swing phase. This deficit causes alterations of the gait, but animals are able to regain a tripod gait after the perturbation. The tibio-tarsal joint angle in individuals with `tarsus catch' was significantly less than in intact animals. Structural defects were consistently associated with `tarsus catch'. The tracheal tubes in the tarsus and around the tibio-tarsal joint were often discolored and the tarsal pads were hardened in aged cockroaches. All aged individuals were able to climb. However, prior to climbing, some animals with `tarsus catch' failed to show postural changes that are normally seen in young animals. Aged individuals can right as rapidly as 1-week-old adults. However, animals with `tarsus catch' take longer to right than aged intact individuals. Old cockroaches have difficulty climbing an incline of 45°, and leg slipping is extensive. Slipping may be caused by tarsal degeneration, but animals that are unsuccessful in inclined walking often show uncoordinated gaits during the attempt. Escape behavior was examined in aged American cockroaches (Periplaneta americana). They do not show normal escape. However, after decapitation, escape movements return, suggesting that degeneration in head ganglia may actually interfere with escape. These findings provide evidence for age-related changes both in the periphery and in the central nervous system of cockroaches and stress the importance of multi-level approaches to the study of locomotion.

[1]  J. Caston,et al.  Motor skills and motor learning in Lurcher mutant mice during aging , 2001, Neuroscience.

[2]  R. Elble,et al.  The syndrome of senile gait , 1992, Journal of Neurology.

[3]  A. Kerin,et al.  Molecular basis of osteoarthritis: biomechanical aspects , 2002, Cellular and Molecular Life Sciences CMLS.

[4]  George E. Stelmach,et al.  Sensorimotor impairment in the elderly , 1993 .

[5]  Oliver Betz,et al.  Performance and adaptive value of tarsal morphology in rove beetles of the genus Stenus (Coleoptera, Staphylinidae). , 2002, The Journal of experimental biology.

[6]  Full,et al.  Maximum single leg force production: cockroaches righting on photoelastic gelatin , 1995, The Journal of experimental biology.

[7]  N. Milgram,et al.  Age-dependent decline in locomotor activity in dogs is environment specific , 2002, Physiology & Behavior.

[8]  T. Scimonelli,et al.  Age-Related Changes in Grooming Behavior and Motor Activity in Female Rats , 1999, Physiology & Behavior.

[9]  J. T. Griffiths,et al.  Fecundity, Longevity, and Parthenogenesis of the American Roach, Periplaneta americana L. , 1942, Physiological Zoology.

[10]  R. S. Sohal,et al.  Insect aging. Strategies and mechanisms. , 1986 .

[11]  Yvan Pelletier,et al.  Behavioural and physical reactions of the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) walking on a slanted surface , 2001, Biological Cybernetics.

[12]  É. Le Bourg The rate of living theory. Spontaneous locomotor activity, aging and longevity in Drosophila melanogaster. , 1987, Experimental gerontology.

[13]  M. Woollacott,et al.  Attentional demands and postural control: the effect of sensory context. , 2000, The journals of gerontology. Series A, Biological sciences and medical sciences.

[14]  P. Hillerås,et al.  Activity patterns in very old people: a survey of cognitively intact subjects aged 90 years or older. , 1999, Age and ageing.

[15]  S. Zill,et al.  Active signaling of leg loading and unloading in the cockroach. , 1999, Journal of neurophysiology.

[16]  R. Ritzmann,et al.  Motion analysis of escape movements evoked by tactile stimulation in the cockroach Periplaneta americana. , 1994, The Journal of experimental biology.

[17]  B. Ulfhake,et al.  Loss of primary sensory neurons in the very old rat: Neuron number estimates using the disector method and confocal optical sectioning , 1998, The Journal of comparative neurology.

[18]  S. Zill,et al.  Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered , 2001, Journal of Comparative Physiology A.

[19]  A comparison of the escape behaviors of the cockroaches Blaberus craniifer and Periplaneta americana. , 1986, Journal of neurobiology.

[20]  L. Roth,et al.  Observations on Reproduction and Development in Cockroaches , 1958 .

[21]  J Kien,et al.  Preparation and execution of movement: parallels between insect and mammalian motor systems. , 1992, Comparative biochemistry and physiology. Comparative physiology.

[22]  L. Larsson,et al.  Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. , 2001, American journal of physiology. Cell physiology.

[23]  G. Mcclearn,et al.  Differences in locomotor activity across the lifespan of Drosophila melanogaster☆ , 1999, Experimental Gerontology.

[24]  Jeffrey M. Camhi,et al.  Behavioral switching in cockroaches: transformations of tactile reflexes during righting behavior , 2004, Journal of comparative physiology.

[25]  Christopher M. Comer,et al.  Identified nerve cells and insect behavior , 2001, Progress in Neurobiology.

[26]  J. T. Watson,et al.  Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis : I. Slow running , 1997, Journal of Comparative Physiology A.

[27]  Full,et al.  Many-legged maneuverability: dynamics of turning in hexapods , 1999, The Journal of experimental biology.

[28]  K G Pearson,et al.  Neural adaptation in the generation of rhythmic behavior. , 2000, Annual review of physiology.

[29]  H. Cruse,et al.  Mechanisms of coupling between the ipsilateral legs of a walking insect (Carausius morosus) , 1988 .

[30]  R. Full,et al.  Three-dimensional kinematics and limb kinetic energy of running cockroaches. , 1997, The Journal of experimental biology.

[31]  Roy E. Ritzmann,et al.  Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics , 2002, Journal of Comparative Physiology A.

[32]  J. Duysens,et al.  Load-regulating mechanisms in gait and posture: comparative aspects. , 2000, Physiological reviews.

[33]  R. Ritzmann,et al.  Descending influences on escape behavior and motor pattern in the cockroach. , 2001, Journal of neurobiology.

[34]  Paul S. G. Stein Neurons, networks, and motor behavior , 1999 .

[35]  J. Camhi,et al.  A modified walking rhythm employed during righting behavior in the cockroachGromphadorhina portentosa , 2004, Journal of comparative physiology.

[36]  J. Andersen Muscle fibre type adaptation in the elderly human muscle , 2003, Scandinavian journal of medicine & science in sports.

[37]  B. E. Maki,et al.  Postural control in the older adult. , 1996, Clinics in geriatric medicine.

[38]  A K Tryba,et al.  Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. , 2000, Journal of neurophysiology.

[39]  B. Ulfhake,et al.  Impairment of peripheral sensory innervation in senescence , 2002, Autonomic Neuroscience.

[40]  J. M. Camhi,et al.  Escape behavior in the cockroach: Distributed neural processing , 1988, Experientia.

[41]  B E Maki,et al.  Age-related changes in compensatory stepping in response to unpredictable perturbations. , 1996, The journals of gerontology. Series A, Biological sciences and medical sciences.

[42]  Lars Farde,et al.  Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain , 2000, Neurobiology of Aging.

[43]  J. Curtsinger,et al.  Locomotor activity as a function of age and life span in Drosophila melanogaster overexpressing hsp70 , 2001, Experimental Gerontology.

[44]  A. Tofilski Senescence and learning in honeybee (Apis mellifera) workers. , 2000, Acta neurobiologiae experimentalis.

[45]  M. Kern Brain Aging in Insects , 1986 .

[46]  S. Zill,et al.  Elasticity and movements of the cockroach tarsus in walking , 1999, Journal of Comparative Physiology A.

[47]  Norman Lewis,et al.  The Longevity of starved Cockroaches. , 1957 .

[48]  T. Rantanen,et al.  Muscle strength, disability and mortality , 2003, Scandinavian journal of medicine & science in sports.

[49]  David D. Thomas,et al.  Force generation, but not myosin ATPase activity, declines with age in rat muscle fibers. , 2002, American journal of physiology. Cell physiology.

[50]  A. Hilliker,et al.  Motorneurons, reactive oxygen, and life span in Drosophila☆ , 1999, Neurobiology of Aging.

[51]  S. Zill,et al.  Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches , 2001, Journal of Comparative Physiology A.

[52]  Thomas Berkefeld,et al.  Age-related changes in primary somatosensory cortex of rats: evidence for parallel degenerative and plastic-adaptive processes , 2002, Neuroscience & Biobehavioral Reviews.

[53]  É. Bourg The rate of living theory. Spontaneous locomotor activity, aging and longevity in Drosophila melanogaster , 1987, Experimental Gerontology.

[54]  T. Aigner,et al.  Molecular pathology and pathobiology of osteoarthritic cartilage , 2002, Cellular and Molecular Life Sciences CMLS.

[55]  S. Gorb,et al.  Roughness-dependent friction force of the tarsal claw system in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). , 2002, The Journal of experimental biology.

[56]  R. Ritzmann,et al.  Motion analysis of leg joints associated with escape turns of the cockroach, Periplaneta americana , 1992, Journal of Comparative Physiology A.

[57]  B. Amblard,et al.  Strategies of segmental stabilization during gait in Parkinson’s disease , 1999, Experimental Brain Research.

[58]  S. Grillner,et al.  The intrinsic function of a motor system — from ion channels to networks and behavior 1 1 Published on the World Wide Web on 22 November 2000. , 2000, Brain Research.

[59]  Y. Jiao,et al.  Adhesion measured on the attachment pads of Tettigonia viridissima (Orthoptera, insecta). , 2000, The Journal of experimental biology.

[60]  R. Ritzmann The neural organization of cockroach escape and its role in context-dependent orientation , 1993 .

[61]  N. Volkow,et al.  Association between decline in brain dopamine activity with age and cognitive and motor impairment in healthy individuals. , 1998, The American journal of psychiatry.

[62]  What is the Cause of the Ageing Atrophy? Assessment of the Fiber Type Composition in Whole Human Muscles , 1993 .

[63]  P. Carlson-Kuhta,et al.  Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. , 1998, Journal of neurophysiology.