In all animals, the aging process is accompanied by
physiological and behavioral changes. Physiological changes,
such as those associated with the nervous and musculoskeletal
systems, often result in decreased or impaired locomotion in
aged individuals (Fernandez et al., 1999; Hilleras et al., 1999;
Le Bourg, 1987; Minois et al., 2001; Scimonelli et al., 1999;
Siwak et al., 2002).
Age-related locomotor deficits are often the result of
degeneration in the central and/or peripheral nervous systems.
In mammals, loss of neurons and neurotransmitters in cortex
and cerebellum can be associated with aging and motor
impairment (Hilber and Caston, 2001; Kaasinen et al., 2000;
Volkow et al., 1998). Sensory information from the limbs is
important in postural control and reactions to perturbations
(Maki and McIlroy, 1996; McIlroy and Maki, 1996).
Degeneration in the peripheral nervous system could result in
loss of vibration or cutaneous sense in the limbs and a decrease
in the response time of reflexes (Shumway-Cook and
Woollacott, 2000; Ulfhake et al., 2002).
Locomotor deficits in aged individuals can also be caused
by non-neural degeneration in the musculoskeletal system.
Aging is frequently associated with weakness and decreased
mass in the muscles (Anderson, 2003). Muscle weakness in the
elderly has been attributed to a reduction in the sliding speed
of cross-bridging elements (Hook et al., 2001; Lowe et al.,
2002). Muscle atrophy with aging is the result of a loss in the
number of muscle fibers, rather than a reduction in fiber size
(Lexell, 1993). Stiffness at the joints and ligaments, which can
be caused by increases in collagen fiber cross-linkages and loss
of elastic fibers, can also result in a decrease in the range of
motion in aged individuals (Aigner and McKenna, 2002; Kerin
et al., 2002).
Insects provide a useful model system for aging studies
because they are short-lived compared with mammals.
Decreases in spontaneous activity with increasing age have
been well documented in fruitflies and honeybees (Fernandez
et al., 1999; Minois et al., 2001; Parkes et al., 1999; Tofilski,
2000). However, none of these papers have examined changes
4453 The Journal of Experimental Biology 206, 4453-4465
© 2003 The Company of Biologists Ltd
doi:10.1242/jeb.00714
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.
Movies available on-line.
Key words: senescence, walking, arthropod, central nervous system,
kinematics.
Summary
Introduction
Effects of aging on behavior and leg kinematics during locomotion in two species
of cockroach
A. L. Ridgel*, R. E. Ritzmann and P. L. Schaefer
Department of Biology, Case Western Reserve University, Cleveland, OH 44106, USA
*Author for correspondence (e-mail: alr17@cwru.edu)
Accepted 8 September 2003