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Sensory Systems in the Control of Movement

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Abstract

Animal movement is immensely varied, from the simplest reflexive responses to the most complex, dexterous voluntary tasks. Here, we focus on the control of movement in mammals, including humans. First, the sensory inputs most closely implicated in controlling movement are reviewed, with a focus on somatosensory receptors. The response properties of the large muscle receptors are examined in detail. The role of sensory input in the control of movement is then discussed, with an emphasis on the control of locomotion. The interaction between central pattern generators and sensory input, in particular in relation to stretch reflexes, timing, and pattern forming neuronal networks is examined. It is proposed that neural signals related to bodily velocity form the basic descending command that controls locomotion through specific and well‐characterized relationships between muscle activation, step cycle phase durations, and biomechanical outcomes. Sensory input is crucial in modulating both the timing and pattern forming parts of this mechanism. © 2012 American Physiological Society. Compr Physiol 2:2615‐2627, 2012.

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Figure 1. Figure 1.

Ensemble cycle averages of the firing of γs and γd motoneurons (A and B), recorded in the common peroneal nerve innervating the ankle flexor tibialis anterior (TA) during spontaneous locomotion in the high decerebrate cat. (A) Three simultaneously recorded γs motoneurons in two cats (panels a and b), in each case an average of 20 step cycles aligned to TA length minima (thick vertical dashed line) and normalized in time. (i) TA electromyogram (EMG: continuous line), medial gastrocnemius (MG) EMG (dotted line), (ii) ankle angle corresponding to TA shortening upward, and (iii) mean firing rate of the γs motoneurons. Mean cycle times in (a) 640 ms and in (b) 800 ms. The three thin vertical dashed lines in A(a) indicate the three phases of TA muscle shortening. B(a) discharge of a γd motoneuron, average of 9 step cycles aligned to TA length minima in each cycle and normalized in time, mean cycle duration 740 ms, B(b) similar data from a γd motoneuron in another cat, average of 12 step cycles with mean duration 735 ms. Note the sudden onset of γd firing at the onset of TA shortening, and the cessation of firing shortly after the start of lengthening. Adapted, with permission, from Figures and 7 in Taylor et al. .

Figure 2. Figure 2.

Ensemble averages of firing rates of group Ia, II, and Ib afferents in ankle extensors (left) and knee flexors (right), recorded during overground locomotion in normal cats. Traces from top to bottom: electromyogram (EMG) and length of receptor‐bearing muscles (lengthening upwards), firing rates of group Ia, II, and Ib afferents. The number of afferents contributing to each average is shown on the right of each firing rate plot. Step cycles were aligned to peaks in either the ankle extensor (triceps surae) or knee flexor (posterior biceps) length signals. The length signals were also used to estimate stance‐swing and swing‐stance transitions in the step cycle (vertical dashed lines). Note the high mean firing rates of Ia and II afferents, indicating high levels of γs drive and the increase in the ankle extensor Ia firing rate prior to the onset of lengthening at the stance to swing transition, compatible with increased γs drive. Derived, with permission, from Figure 6 .

Figure 3. Figure 3.

Estimated time course of joint angle variations computed from the firing rates of 47 sensory afferents recorded simultaneously during treadmill locomotion with a microelectrode array implanted in the L7 dorsal root of a cat. This group included five spindle 10 and five spindle 20 endings, one Golgi tendon organ, four glabrous cutaneous receptors and two hair follicle receptors. Step‐cycle averages of the actual and estimated (A) position, (B) velocity, and (C) acceleration in joint‐angle coordinates. Each plot shows the mean of 162 steps (toe‐off to toe‐off). The thin lines represent ±1 s.d. from the mean of the actual trajectories. The up and down arrows indicate onset of the swing and stance phases, respectively. Reproduced, with permission, from reference .

Figure 4. Figure 4.

Descending control of the locomotor step cycle. (A) Increments in the intensity of stimulation in the midbrain locomotor region (MLR) in the high decerebrate cat (lower trace) increases the cadence of locomotion (upper traces) (adapted, with permission, from reference ). (B) Schematic summarizing the velocity command hypothesis: a command signal specifying desired body velocity descends from brainstem and drives the timing element of the locomotor central pattern generator (CPG) to generate cadences with flexor and extensor phase durations that depend in a specific way on cycle duration. The velocity signal also drives the pattern formation network (PFN) to modulate the amplitudes of activation of the flexor and extensor muscles according to a square law relationship. Muscle displacement automatically modulates muscle force through the intrinsic length‐tension properties. Muscle force and displacement sensed by spindle and tendon organ afferents elicit continuous stretch reflexes as well as modulating or overriding phase transitions via the CPG timer. Presented at the Society of Experimental Biology Annual General Meeting in 2009 .



Figure 1.

Ensemble cycle averages of the firing of γs and γd motoneurons (A and B), recorded in the common peroneal nerve innervating the ankle flexor tibialis anterior (TA) during spontaneous locomotion in the high decerebrate cat. (A) Three simultaneously recorded γs motoneurons in two cats (panels a and b), in each case an average of 20 step cycles aligned to TA length minima (thick vertical dashed line) and normalized in time. (i) TA electromyogram (EMG: continuous line), medial gastrocnemius (MG) EMG (dotted line), (ii) ankle angle corresponding to TA shortening upward, and (iii) mean firing rate of the γs motoneurons. Mean cycle times in (a) 640 ms and in (b) 800 ms. The three thin vertical dashed lines in A(a) indicate the three phases of TA muscle shortening. B(a) discharge of a γd motoneuron, average of 9 step cycles aligned to TA length minima in each cycle and normalized in time, mean cycle duration 740 ms, B(b) similar data from a γd motoneuron in another cat, average of 12 step cycles with mean duration 735 ms. Note the sudden onset of γd firing at the onset of TA shortening, and the cessation of firing shortly after the start of lengthening. Adapted, with permission, from Figures and 7 in Taylor et al. .



Figure 2.

Ensemble averages of firing rates of group Ia, II, and Ib afferents in ankle extensors (left) and knee flexors (right), recorded during overground locomotion in normal cats. Traces from top to bottom: electromyogram (EMG) and length of receptor‐bearing muscles (lengthening upwards), firing rates of group Ia, II, and Ib afferents. The number of afferents contributing to each average is shown on the right of each firing rate plot. Step cycles were aligned to peaks in either the ankle extensor (triceps surae) or knee flexor (posterior biceps) length signals. The length signals were also used to estimate stance‐swing and swing‐stance transitions in the step cycle (vertical dashed lines). Note the high mean firing rates of Ia and II afferents, indicating high levels of γs drive and the increase in the ankle extensor Ia firing rate prior to the onset of lengthening at the stance to swing transition, compatible with increased γs drive. Derived, with permission, from Figure 6 .



Figure 3.

Estimated time course of joint angle variations computed from the firing rates of 47 sensory afferents recorded simultaneously during treadmill locomotion with a microelectrode array implanted in the L7 dorsal root of a cat. This group included five spindle 10 and five spindle 20 endings, one Golgi tendon organ, four glabrous cutaneous receptors and two hair follicle receptors. Step‐cycle averages of the actual and estimated (A) position, (B) velocity, and (C) acceleration in joint‐angle coordinates. Each plot shows the mean of 162 steps (toe‐off to toe‐off). The thin lines represent ±1 s.d. from the mean of the actual trajectories. The up and down arrows indicate onset of the swing and stance phases, respectively. Reproduced, with permission, from reference .



Figure 4.

Descending control of the locomotor step cycle. (A) Increments in the intensity of stimulation in the midbrain locomotor region (MLR) in the high decerebrate cat (lower trace) increases the cadence of locomotion (upper traces) (adapted, with permission, from reference ). (B) Schematic summarizing the velocity command hypothesis: a command signal specifying desired body velocity descends from brainstem and drives the timing element of the locomotor central pattern generator (CPG) to generate cadences with flexor and extensor phase durations that depend in a specific way on cycle duration. The velocity signal also drives the pattern formation network (PFN) to modulate the amplitudes of activation of the flexor and extensor muscles according to a square law relationship. Muscle displacement automatically modulates muscle force through the intrinsic length‐tension properties. Muscle force and displacement sensed by spindle and tendon organ afferents elicit continuous stretch reflexes as well as modulating or overriding phase transitions via the CPG timer. Presented at the Society of Experimental Biology Annual General Meeting in 2009 .

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Arthur Prochazka, Peter Ellaway. Sensory Systems in the Control of Movement. Compr Physiol 2012, 2: 2615-2627. doi: 10.1002/cphy.c100086