Integrative and Comparative Biology Advance Access originally published online on June 22, 2007
Integrative and Comparative Biology 2007 47(4):457-464; doi:10.1093/icb/icm053
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Contextual learning and obstacle memory in the walking cat
Department of Physiology, University of Alberta, Edmonton, Canada
Correspondence: 1E-mail: keir.pearson{at}ualberta.ca
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Animals in their natural environments display a remarkably diverse variety of walking patterns. Although some of this diversity is generated by alterations in feedback from the moving limbs, animals can modify their walking in many ways that cannot be directly attributed to this sensory feedback. For example, animals and humans can learn to associate a particular environment with disturbances that were experienced there earlier, and alter their stepping accordingly even after the disturbance has ceased. Another relevant example is that walking animals are aware of the locations of obstacles around them, and use this awareness to alter their stepping patterns even when there is no visual information available about the location of the obstacles relative to the body. In this article, we discuss recent work from our laboratory that addresses these two topics. First, we report that perturbing walking cats in a consistent manner evokes long-lasting changes to the walking pattern that are expressed only in the context in which walking was disturbed. Secondly, we show that cats that have stepped over an obstacle remember the location of that obstacle relative to the body during long delays, and can use that memory to guide stepping. The general theme of this research is that sensory inputs that signal context—the visual and auditory environment that surrounds an animal—play an important role in shaping the basic pattern of locomotion.
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To be useful, walking must be adaptable. A stereotyped pattern of stepping movements would be poorly suited to variable environments, which requires animals to step over obstacles, scramble over slippery terrain, and alter leg movements when going uphill or downhill. The neural mechanisms underlying this flexibility are, in general, poorly understood. Obviously, adaptive behavior depends critically on the modification of central pattern generating networks by sensory signals that encode information about the features of the environment. Our knowledge about how the appropriate information is coded in different sensory systems and how this information is processed in the central nervous system is fragmentary for most walking systems. Nevertheless, over the past two decades numerous investigations have demonstrated that cutaneous and proprioceptive signals have powerful influences on central pattern-generating networks in the walking system of the cat, and that these influences are appropriate for mediating adaptive modifications of stepping to avoid obstacles unexpectedly contacting the legs and to compensate for unexpected changes in the supporting surface, respectively. The results of these investigations have been extensively reviewed (Prochazka 1996
; Donelan and Pearson 2004; Rossignol et al. 2006). In addition to cycle-by-cycle modifications of stepping to adjust to the immediate demands of the environment, the characteristics of stepping also depends on the context in which animals are behaving. For example, leg and body movements change depending on whether an animal is stalking prey or avoiding a predator. Similarly, the environmental context in which an animal walks, such as cluttered forest or an open plain, also changes the characteristics of walking. This requires that knowledge of the environment and nearby obstacles derived from visual information and previous experience be used to shape the basic motor output for walking.
In this article, we review recent studies from our laboratory that demonstrate that stepping in the hind legs of walking cats can be modified by contextual cues in the environment and by the memory of the location of obstacles relative to the body. We then discuss which regions of the central nervous system may be involved in mediating these modifications.
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Learning the context of sensory events controls swing in walking cats |
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A consistent feature of locomotion is the ability to adapt the pattern of walking to maintain stability and efficiency in diverse environments (Pearson 2000
). For example, animals can easily adapt to walking up (Carlson-Kuhta et al. 1998) and down (Smith et al. 1998) slopes, walking through cluttered environments (Wilkinson and Sherk 2005), and to walking with unexpected loss of ground support (Gorassini et al. 1994). In some cases, the changes to the basic pattern of walking are so dramatic that they are unlikely to be generated entirely by changes in sensory feedback from the legs. For example, in cats walking up or down steep slopes some flexor muscles in the hind legs that are normally active only during the swing phase change their pattern of activity and become active during the stance phase (Smith et al. 1998). This indicates that central pattern-generating networks in the spinal cord can be strongly influenced by descending signals containing information about the context in which the animal is walking. In addition, numerous studies have reported long-lasting changes in stepping and walking in response to modifications of the environment that persist in the absence of the altered stimuli (Gordon et al. 1995; Prokop et al. 1995; Reynolds and Bronstein 2003). These observations suggest that the flexibility of walking depends to some degree on learning different patterns of locomotion, each appropriate for a particular situation and used when needed.
Recently, our laboratory has completed a series of experiments that provide evidence that supports this hypothesis (McVea and Pearson 2007). These experiments examined the modifications in the swing phase of a hind leg of walking cats in response to repetitive tactile stimuli of the dorsum of the paw. Normally, when the paw of a walking cat strikes an obstacle during the swing of walking, a precise pattern of muscle activity is initiated to quickly lift the foot up and over the obstacle (called the stumbling corrective response). This reflex response is mediated by cutaneous receptors in the paw (Forssberg 1979; Wand et al. 1980). We found that repeatedly evoking a series of stumbling corrective responses led to an increase in knee flexion during the swing phase of walking (which we call hyperflexion) and a significantly higher step in the leg that had repeatedly touched the obstacle, without any change in the stepping of the other three legs (Fig. 1). Importantly, the changes in knee flexion and step height lasted long after the perturbing stimulus had been removed, persisting for many days in some cases. We interpret this as clear evidence that a maintained disturbance in the environment can easily cause long-term changes in components of the system patterning activity in flexor muscles during swing. To test whether this represented a general change in the pattern-generating networks or a new behavior specifically associated with the environment, we evoked the hyperflexion when animals were walking on a treadmill, and then observed their walking in different environments. The persistent hyperflexion was only observed on the treadmill and not when the animal was walking in other contexts (Fig. 1C). This suggested to us that a new stepping pattern which minimized the effect of the perturbing stimuli had been learned and was expressed when appropriate.
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This new stepping pattern was learned very quickly, as the increase in step height generally reached a maximum after only 100–120 sequential stimuli. Moreover, the increase in step height persisted for thousands of undisturbed steps over the following hours and days. The speed at which it was acquired and the persistence of this behavior suggests it may represent an important feature of normal locomotion. Specifically, walking animals may rapidly adapt their pattern of walking to a particular set of environmental conditions and learn this pattern for future use. A number of reports have described consistent, substantial changes to the basic pattern of walking which are expressed in specific contexts. For example, when cats (Carlson-Kuhta et al. 1998
; Smith et al. 1998) and humans (Lay et al. 2006) walk up and down slopes, leg muscles substantially change the timing and magnitude of their activation. These changes vary from muscle to muscle, suggesting that the centrally generated pattern of walking is changed. Similarly, when humans walk on a springy surface, they change their step height and center of mass height, as well as the activity of muscles throughout the legs, to remain as stable as possible (Marigold and Patla 2002, 2005). It is possible that these altered patterns of walking in different environments are learned early in life. Later, as these challenges are encountered again, central structures of the nervous system trigger the appropriate changes to the locomotor output. |
Memory-guided modifications of stepping in walking cats |
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In addition to the environmental context modifying stepping movements in walking animals, remembering and recognizing features of the environment are clearly involved in some aspects of walking, such as navigation and the avoidance of obstacles. A clear example of short-term memory controlling stepping is that neither cats (Fowler and Sherk 2003
) nor humans (Patla and Vickers 1997, 2003) look at obstacles as they step over them. Rather, they look two or three steps ahead, and thus use some form of memory to step at the appropriate time. In cats, this memory of obstacles in the environment has been shown to last for the duration of about four steps (Wilkinson and Sherk 2005). Quadrupeds have the additional problem of guiding a second set of legs to step over an obstacle after the head and eyes are well past (Fig. 2). We have recently begun to explore this process (McVea and Pearson 2006). Initially, we wanted to know whether the hind legs were guided by the same form of memory that guides locomotion in the absence of visual feedback (Patla 1998; Wilkinson and Sherk 2005). We tested this by developing an experiment protocol in which cats stepped over an obstacle with the forelegs, but not the hind legs, so that the obstacle was straddled between the two sets of legs (Fig. 2A). We then maintained the cats in this position for a variable delay period, during which they focused their attention on a food dish. At the beginning of the delay period, the obstacle was quietly lowered. At the end of the delay period, we allowed the cats to continue walking forward and the trajectory of their hind legs indicated whether they remembered the position of the obstacle between their front and hind legs. Because the obstacle had been removed, any deviations from a normal step profile would not be due to cutaneous or visual feedback, but would be generated by a memory of the obstacle. We were surprised to discover that the memory of the obstacle persisted for as long as we could keep the animals standing in the straddling position (Fig. 2B). Even after 10 min, in one case, the step over the location the cat had seen the obstacle was much higher than normal, indicating the cat remembered the presence of the obstacle. This is in sharp contrast to the much shorter memories of obstacles normally observed during locomotion, which last on the order of 1–10 s (Patla and Vickers 1997; Wilkinson and Sherk 2005).
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Could the memory we observed be so long-lasting because it is imprecise? Could the cats, for example, simply be remembering that there was something between their front and hind legs, without knowing anything about its size or exact location? Later experiments ruled out this possibility. The step following the delay period was adjusted to the height of the obstacle, and to the position of the obstacle relative to the foot. Furthermore, when we repeated the experiment with cats straddling two obstacles, they clearly remembered the size and location of both, because they often stepped over one and then over the original position of the second. In some cases, the movement of the leg was changed in a very sudden and striking way to avoid the remembered position of the obstacle.
These observations are strong evidence that the hind legs of walking cats are guided by precise and long-lasting memories of obstacles. One distinguishing feature about the movements of the hind legs is that there is an additional source of information available about the obstacle when they step, namely the movement of the forelegs which have already stepped over the obstacles. To test whether the movement of the forelegs over an obstacle contributed to the establishment of the memory that guides hind leg stepping, we repeated the experiment described earlier, except that we stopped the cats before either the forelegs or the hind legs had stepped over the obstacle (Fig. 3). After a variable delay period (during which the obstacle was lowered into the ground), we moved the cats forward, noting the step height of both sets of legs as the cats passed over the previous location of the obstacle. We were careful to ensure that the cats did not see the obstacle being lowered. In this case, steps after a delay of anything more than about 20 s were usually not higher than steps when there was no obstacle, indicating that the animal did not form a long-lasting memory of the obstacle (Fig. 3). This simple result suggests that the movement of the forelegs over an obstacle contributes to a long-lasting memory of the obstacle which is used to guide the hind legs at the appropriate time in the future.
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Neuronal structures mediating contextual and memory-related changes in stepping |
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Our findings that stepping in the cat can be readily modified for long periods of time by interactions with obstacles in the environment (previous sections) raise the question of what neuronal systems are responsible for mediating these modifications. Because the characteristics of the two modifications we have described are quite different, we will consider each separately.
Modification of stepping by environmental context
A striking feature of the maintained hyperflexion produced by repetitively stimulating one hind paw was that it was only expressed in the environmental context in which the stimuli were applied (Fig. 1B). We made no attempt to rigorously determine what features of the environment were critical for evoking hyperflexion, but it is likely that multiple features are involved and that these are not necessarily the same in all animals. For instance, depending on the animal, hyperflexion could be initiated by the introduction of the stimulating probe without touching the paw, by touching the contralateral leg, and by setting the treadmill speed to the value close to the speed when the hyperflexion was conditioned (McVea and Pearson 2007). These multiple factors, and the variation between animals, immediately suggests that high-level neuronal systems are involved in mediating the hyperflexion. This is consistent with the fact that hyperflexion was not observed in conditioned animals following decerebration, and that long-lasting hyperflexion could not be evoked in decerebrate walking animals (McVea and Pearson 2007).
What then is the identity of these high-level systems? Currently, we can only speculate in the most general way on this issue. One possibility is systems in the medial temporal lobe. Numerous studies in rodents have demonstrated that structures within the medial temporal lobe, especially the hippocampus and associated areas, are necessary for recognizing the environmental context in which an aversive stimulus (e.g., electric shock to the feet, unpleasant food, etc.) has been experienced (Holland and Bouton 1999; Jeffery et al. 2004). In our study the stimulus was quite mild, but if we consider it as aversive (i.e., a stimulus to be avoided) then the parallel with the environmentally conditioned avoidance in rodents is striking. The main evidence that structures in the medial temporal lobe are involved in contextual learning is that the learning is impaired by hippocampal lesions (Maren and Fanselow 1997; Maren et al. 1997; Aguado et al. 1998). The importance of environmental context in the expression of learned behavior has also been found in the classically conditioned eye-blink response in rabbits (Penick and Solomon 1991). Transferring the animals to an environment different from that in which it was conditioned disrupts conditioning, but this disruption does not occur in animals with hippocampal lesions, thus supporting the notion that the hippocampus plays a major role in contextual learning. Currently, we have no evidence that structures in the medial temporal lobe in the cat are critical for mediating the conditioned hyperflexion of the hind leg in response to repeated stimulation of the paws. Surprisingly, few studies have examined the influences of disrupting the function of the hippocampus on the behavior of cats (Irle 1985), and no single-unit recordings have been made from the hippocampus in walking cats. The conditioned hyperflexion we have discovered may be a useful paradigm for examining the role of the hippocampus in contextual learning in cats.
Other brain structures that may be important is signaling the context for modifying the hyperflexion are the basal ganglia. The anatomy and electrophysiology of neurons in the basal ganglia of primates has led to the suggestion that a "function of the basal ganglia ... is to acquire learned representations of contexts and to train the frontal cortex to produce appropriate behaviors in the presence of such contexts" (White 1997). Furthermore, it is generally accepted that the basal ganglia are also involved in the formation of consistent relationships between stimulus cues and behavioral responses, usually referred to as habit formation (Yin and Knowlton 2006). It is not unreasonable to consider the conditioned hyperflexion as a habit formed by the tactile stimuli, since this response persists, i.e., becomes habitual, long after the antecedent stimuli have been removed.
Although it is obvious that supraspinal regions are necessary for establishing the conditioned hyperflexion (since it cannot be conditioned in decerebrate animals), it is possible that modifications do occur in structures within the brain stem, including the cerebellum and spinal cord. The effects of these modifications may be expressed only in the presence of the appropriate context-related signals from the forebrain.
Modification of stepping by knowledge of obstacle location
Our observations on cats stepping over obstacles have clearly demonstrated that a memory of the location of an obstacle relative to the body can precisely guide the trajectories of the hind legs during the swing phase. This form of memory can last many minutes if one or both forelegs step over the obstacle (Fig. 2). The necessary signal from the forelegs for establishing the memory has not been identified, but it is either a feedback signal from proprioceptors or a feedforward signal related to the motor commands controlling foreleg swing (called efference copy) (Nelson 1996; Wolpert and Ghahramani 2000; Flanagan et al. 2003), or a combination of both. In addition, the memory can be established by a tactile signal from a foreleg if a foreleg strikes the obstacle during swing in the absence of vision (unpublished observations). Thus establishing the memory of obstacle location is a flexible process that can involve multiple sensory signals (visual, proprioceptive, tactile) and perhaps signals related to motor commands. We expect, therefore, that the neuronal system establishing and maintaining memories of obstacle location should be capable of integrating information from all these sources.
One brain region that has this capability is the posterior parietal cortex, PPC (Hyvarinen 1982; Graziano and Cooke 2006). The PPC consists of a number of discrete regions that include areas 5 and 7 and multiple regions in and around the intraparietal sulcus (see review by Battaglia-Mayer et al. 2006). Area 5 is especially interesting because it receives input from visual, cutaneous, and muscle receptors, and in monkeys neurons in this region are activated when the animals make reaching movements into immediate extrapersonal space (Hyvarinen 1982). The combination of visual and proprioceptive signals in this region is considered to contribute to the internal representation of position of the body and limbs (Graziano 1999), a concept that is supported by the loss of awareness of limb position in patients with damage to the PPC (Hyvarinen 1982; Wolpert et al. 1998). Of special interest in the current context is that many neurons in area 5 of monkeys are active during the delay period of an instructed-delay task, and this activity is a function of the intended direction of arm movement (Kalaska et al. 2003). Thus, neurons in this region may contribute to a representation of a memory for an instructed movement in addition to their possible role in the internal representation of body and limb positions.
Based on these and other observations in monkeys and humans it is reasonable to suppose that area 5 in the PPC of cats could be involved in remembering the location of obstacles relative to the body and/or guiding the movements of the legs to avoid these obstacles. The results from a recent lesion study (Lajoie and Drew 2007) are consistent with this notion. Unilateral lesions of area 5 were found to reduce the ability of walking cats to step cleanly over obstacles and to correctly place the paws when approaching the obstacles. Similarly, an earlier study (Fabre and Buser 1981) reported that lesions in the anterior sylvian cortex (likely including parts of area 5) caused deficits in visually guided reaching movements of the forelegs to a moving target. Drawing firm conclusions about the function of area 5 from these lesions studies in difficult. Obviously, lesions of area 5 produce a form of visual ataxia, but this could be due to the degradation of one or more processes such as the visual representation of obstacle location relative to the body, short-term memory of obstacle location, the internal representation of leg and body position, the planning of leg movements, and the execution of leg movements.
The specific question we would like to resolve is whether neurons in area 5 are involved in the memory task we have described in the previous section (Fig. 2). If they are, then one simple prediction is that the bilateral inactivation (lesion or chemical) should degrade the memory of obstacle location. This experiment has not yet been performed. Another prediction is that activity in neurons in area 5 should be correlated with some features of the memory task, such as a maintained increase or decrease in activity while the animal is straddling the obstacle. Only two studies have recorded neuronal activity in area 5 of walking cats (Beloozerova and Sirota 2003; Lajoie and Drew 2006). Both reported elevated activity when animals step over obstacles, and one (Lajoie and Drew 2006) reported that some neurons remained active as obstacles pass under the body of the animal. This observation suggested that these neurons might be involved in coordinating the stepping of the fore- and hind-legs over the obstacles. Since coordination of stepping over obstacles requires a short-term memory of obstacle location (see previous section), then it is plausible that these neurons play a role in the representation of the memory. Stronger support for this conclusion has come from recent studies in Dr Trevor Drew's laboratory that have found that when animals stop walking so that their fore- and hind-legs straddle an obstacle, many neurons in area 5 substantially increase their activity for the entire period the animal is straddling the obstacle (Drew, personal communication). Whether or not these neurons are directly involved in regulating the changes in movements of the hind legs to avoid the obstacle is unknown at present. An alternative possibility is that the neurons are part of a representation of the location of the obstacle relative to the body that might be used for an entirely different purpose,such as a general representation of the external environment.
Obviously we at a very early stage in exploring the neuronal basis of the memory task described in the previous section. Recent observations on the activity in area 5 of the PPC are very promising, but they clearly have to be extended before any definite conclusions can be drawn regarding their role in modifying leg movements to avoid obstacles. Even if it is eventually concluded that neuronal systems in area 5 are essential for the representation of memories for obstacle location, the challenging task of determining how this stored information is accessed will remain. Almost certainly, the solution to this problem will require detailed exploration of activity of other regions of the brain during the memory task, such as premotor areas, motor nuclei in the thalamus, the cerebellum, and basal ganglia. Examination of premotor areas may prove to be especially interesting since neurons in these regions in primates have been shown to code the locations of objects in the dark (Graziano et al. 1997) and to receive efference copy of eye-movement commands (Sommer and Wurtz 2004). The latter is relevant to our studies because the long-term maintenance of the memory of obstacle location requires the forelegs to step over the obstacle, suggesting that efference copy of foreleg commands could be involved in maintenance of the memory.
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Conclusions |
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The central theme of this review has been that the basic pattern of locomotion in walking animals is modified in response to the context in which walking occurs. This modification is predictive, that is, it optimizes locomotion for the task at hand, and does not rely on feedback from the limbs. In some cases, as in the persistent hyperflexion described in the first section of this review, changes to the walking pattern are learned following repeated disturbances in a particular environment. We believe that other instances of changes to the basic locomotor output, such as those that occur when walking up and down slopes, and on compliant substrates, may be motor patterns that have been learned to maximize stability and efficiency under constraints that differ from those present during level walking.
Locomotion is also modified to accommodate obstacles and obstructions in the environment. This is a complex process, as vision is rarely used to guide foot placement directly. Instead, some form of memory of the position of obstacles relative to the body is used. This memory must be sufficiently detailed to prevent the possibility of errors, and it must also be updated as obstacles move relative to the feet and the body during locomotion.
We can only speculate about what regions of the nervous system are involved in these processes. Visual input regions such as the suprasylvian area, and output regions such as the motor cortex, are certain to be involved. Between these regions many parts of the cortex are needed to recognize and remember features of the environment and select the appropriate motor pattern in response. We think that area 5 of the parietal cortex is a good candidate, particularly in the process of guiding the hind legs of walking cats over obstacles, but experiments to confirm this are only just beginning. Nonetheless, we hope this research will help to focus attention on the complex problem of how prior experiences, visual information, spatial memories and behavioral state, along with feedback from the moving limb, are integrated into the basic pattern of locomotion to produce the diverse patterns of stepping in walking animals.
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Footnotes |
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From the symposium "Recent Developments in Neurobiology—A Tribute to Professor Douglas G. Stuart" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
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