Psychophysical methods for study of sensory-motor behavior using a food-carrying (hoarding) task in rodents

Rodents (rat, mouse, gerbil) display species-typical food-handling movements that are dependent upon features of the food they are given. They swallow small pieces of food directly, eat medium-sized pieces from their forepaws, and carry (hoard) large pieces of food to refugees for consumption or storage. Both food size and anticipated eating time influence the occurrence of a given movement. Response speeds are also influenced by food size. The latency to initiate food-carrying and travel-speed during food-carrying are inversely related to the size of food, while the latency to return to the food source for more food is directly related to the amount of food just eaten. Using menu-driven computer programs, event relays and photocells, and videorecording methods, the food handling movements can be both monitored and quantified. Use of the method is illustrated by showing how manipulations such as familiarity with the environment, environmental lighting, food pellet size and peripheral and central processes influence movements and response speeds. The procedure provides a useful way to study sensorimotor processes, motivation and reinforcement processes, and memory and cognitive processes used in foraging.     

Disruption of central cholinergic systems in the rat by basal forebrain lesions or atropine: effects on feeding, sensorimotor behaviour, locomotor activity and spatial navigation

Rats with ibotenic acid lesions of the nucleus basalis magnocellularis, the origin of the extrinsic cholinergic innervation of the cortex, were examined for changes in feeding, sensorimotor behaviour, nocturnal locomotor activity, and place navigation in the Morris swimming pool task, in comparison with control rats and rats receiving the muscarinic antagonist, atropine. The lesions produced acute feeding impairments, marked by weight loss and vigorous active rejection of food and water lasting 2-4 days, sensorimotor impairments in placing and orienting, and overnight hyperactivity. A similar hyperactivity was induced by atropine, lasting approximately 6 h following the injection. Rats with lesions or receiving atropine were similarly impaired in the acquisition of the spatial navigation task, they failed to reach control levels of efficiency even once they had acquired the task, and they showed small but significant retention impairments when pretrained in the absence of either treatment. The results are discussed in terms of the lesions producing a disruption of cortical cholinergic systems, with implications for the clinical disorder of senile dementia of the Alzheimer type, and in terms of possible associated disruption to non-cholinergic systems.     

Precision grasps of children and young and old adults: individual differences in digit contact strategy, purchase pattern, and digit posture

The evolutionary origins and variations of the precision grip, in which an object is held between the thumb and other digits, are poorly understood. This is surprising because the neural basis of this grasp pattern, including the motor cortex and pyramidal tract have received extensive study. Most previous work has shown that features of an object to be grasped (external factors) determine grasp patterns. The objective of the present study was to investigate individual differences (central factors) in use of the pincer and other precision grips. The grasping patterns of male and female young adults, older adults and children were examined as they reached (with both left and right hand) for five small beads (3-16 mm diameter). Frame-by-frame analysis of grasping indicated a high degree of variability in digit contact strategies, purchase patterns and digit posture both within and between subjects. (1) The contact strategies consisted of five variations, depending on whether the thumb or the index finger dragged or stabilized the bead for grasping. (2) Purchase patterns consisted of seven different types of precision grips, involving the thumb and various combinations of other digits. (3) There were four variations stemming from the posture of the non-grasping digits. Grip patterns of the left and right hands were correlated in individual subjects, as were strategies used for different bead sizes. Females displayed slightly more variability in grasp patterns than did males, and digit width (obtained from photocopies of the subjects' hands) was weakly correlated with the grasp patterns used. Although it was expected that the pincer would be used for all objects, it was preferentially used for only the smallest object except for older adults who used the pincer grasp on most objects. The variability in digit contact strategies, purchase patterns, and posture of the non-grasping digits indicates that central factors (innate or learning-induced architecture of the left parietal cortex) make important contributions to the selection of a grasping pattern. These individual differences are discussed in relation to the neural control of grasping and its potential contribution to understanding the evolution, development, and pathology of the precision grip.     

Preserved ipsilateral-to-lesion motor map organization in the unilateral 6-OHDA-treated rat model of Parkinson's disease

The classic view of dopamine (DA) loss in Parkinson's disease is that it produces a functional deafferentation in striatal-cortical circuitry that, in turn, contributes to sensorimotor deficits. The present study examines this view in the rat by assessing how DA-depletion affects the intracortical microstimulation (ICMS) topographic representation of movement in the rostral and caudal motor areas of the motor cortex. The ICMS map is used as an index of motor cortex function because it has been shown to reflect motor function and experience. Groups of rats received no training or skilled reach training and were then given unilateral 6-hydroxydopamine (6-OHDA) or sham lesions of the nigrostriatal bundle to deplete nigrostriatal DA. Lesion success was confirmed by abnormalities in skilled reaching, by apomorphine-induced rotation, and by loss of DA neurons in the substantia nigra. The size and threshold of the motor map in naive and skilled reach trained DA-depleted rats were preserved. In addition, there was an increase in distal limb representation in the caudal forelimb area (CFA) in the DA-depleted rats suggesting a possible plastic response to the behavioral effects of DA-depletion. The presence of preserved size and modified map organization in DA-depleted rats is discussed in relation to the hypothesis that preserved motor cortex functionality despite DA loss underlies the spared motor abilities of DA-depleted rats.     

Long-Evans and Sprague-Dawley rats have similar skilled reaching success and limb representations in motor cortex but different movements: some cautionary insights into the selection of rat strains for neurobiological motor research

Many rat strains are used for neurobiological studies of nervous system function and behavior. The most widely used strain for studies of the neural basis of movement is the out bred, pigmented Long-Evans strain, while the most widely used strains for the study of movement impairments in neurological disease are out bred albino rats, including Sprague-Dawley rats. Although previous research has indicated that there are strain differences in skilled movements displayed by different rat strains, there has been no explicit comparison of the Long-Evans and Sprague-Dawley strains. This was the purpose of the present study. The rats were video recorded as they learned to reach for single food pellets and the video records were subjected to frame-by-frame analysis. Component movements of reaching were scored using a system derived from Eshkol-Wachman Movement Notation (EWMN). The quality of movements was described using Laban Movement Analysis (LMA). Forelimb representations in motor cortex were defined electrophysiologically. Acquisition scores and success in reaching did not differ between the two strains, nor did the topographical representation of the forelimb in motor cortex. Long-Evans and Sprague-Dawley rats did differ in the movements used for reaching and on the quality of their movements. The movements of Sprague-Dawley rats resembled the movements of Long-Evans rats with motor system injury. That rat strains can show both quantitative and qualitative differences in movement is useful for the understanding of the genetic, neural, and behavioral organization of the motor system. The results are also relevant to the question of appropriateness of particular rat strains for studies of neurological diseases and the effects of albinism on motor behavior, and suggest that some of the most widely used rat strains for neurological investigations may be less than appropriate.     

Did a change in sensory control of skilled movements stimulate the evolution of the primate frontal cortex?

The classical view of the evolution of such skilled movements as use of the hand and digits for reaching and grasping posited that these movements had their origin in the primate lineage. The hypothesis was that the permissive influence of adaptations to an arboreal environment led to the evolution and elaboration of these skills. Associated with skilled movements were increases in the size of the frontal lobe, temporal lobe, and cerebellum and the elaboration of new connections between these structures and other cortical regions, the brainstem, and spinal cord. The classical view saw rodents as phylogenetically old and relatively unrelated animals, displaying no skilled movements, and whose normal repertoire of behavior had little dependence on the frontal lobes. Here, evidence is reviewed that shows that the classical view of the origins of skilled movements is incorrect. Skilled movements are phylogenetically old, evolved in relation to food handling, and are especially well developed in rodents. Behavioral evidence also shows that the skilled movements of rodents are dependent upon the function of the frontal cortex. Nevertheless, there are difference in the sensory control of skilled movement in primates and rodents. Skilled movements are largely directed by vision in primates but are directed by hapsis/olfaction in rodents. This difference in sensory control suggests that at a dividing point between primates and rodents, there was a profound behavior/brain transformation. Primates retained the skilled movements exemplified in rodents, but brought these movements under visual control. Correspondingly, along with many other anatomical changes, the primate frontal cortex became relatively larger and move complex under visual influence.     

The thermal control of immobility in developing infant rats: Is the neocortex involved?

Infant rats aged 1 to 5 days lose heat rapidly when first exposed to room temperature; they also are initially very active and cannot be immobilized when turned over onto their sides and restrained for a few seconds. However, once core temperature drops closer to ambient levels, the stimulus for movement (rapid loss of heat from skin to environment) is diminished and immobility occurs. If the rapid heat loss, a source of apparent spontaneity, is prevented by precooling or continuous warmth, activity is blocked and prolonged restraint-related immobility can be readily produced. The warmed pups frequently made small twitches typical of those associated with paradoxical sleep. By 10 days, the pups can no longer be immobilized on their sides when pre-cooled, possibly because motor subsystems related to shivering thermogenesis (i.e., behaviors, including righting, that actively maintained a crouched upright position) begin to develop. At this age the pups can still be immobilized when warmed, but by 25 days of age slight warming is no longer effective because of the emergence of other sources of spontaneous locomotion that cannot be blocked by warmth, and/or because warmth can no longer induce paradoxical sleep. To test for the influence of the developing neocortex on immobility, pups were decorticated at 6 days of age. The activity and restraint immobility durations of the decorticate pups were not different from controls under any thermal condition at any postoperative age. Warmth-induced immboility was present following decortication in adult rats, but only in the early postoperative days, perhaps relating to subcortical diaschisis. It is suggested that the neocortex is not a major inhibitory influence on immobility induced by restraint.     

Decortication abolishes place but not cue learning in rats

The experiments examined whether decorticate rats are able to acquire a place learning strategy, as compared with a cue learning strategy, to successfully navigate from one place to another and whether the hippocampus, in the absence of the neocortex, contributes to successful performance. Decorticate rats, with or without hippocampectomy, were unable to locate an “invisible” platform submerged at a fixed place in a tank of cool water (made opaque by milk), rather they scrabbled at the edges of the tank and failed even to initiate search strategies. They were able to learn to swim directly to the platform if it was visible. Their ability to find the hidden platform was not enhanced by presurgical experience or two-stage ablations with training before and after ablations. When pretrained on the cue task and tested on the place task, they learned to inhibit scrabbling at the tank edges and “search” in a haphazard fashion for the hidden platform, but they never learned to swim directly toward it. When decorticate rats, trained on the cue task, received superior colliculus or basal ganglia removal in a second operation, cue learning was abolished. Hippocampal removal after decortication left performance on the cue task unaffected. The results demonstrate: (1) the integrity of the neocortex is essential for place learning; (2) the brainstem, including superior colliculus and basal ganglia, is sufficient for cue learning; and (3) in the absence of the neocortex the hippocampus plays no role in guiding either type of navigation. It is concluded that sensorimotor subsystems of the forebrain play a special role as detector-response systems for guiding behaviour in response to constellations of distal stimuli, whereas subcortical structures are sufficient for navigation to a single stimulus.     

Effects of kainic acid lesions in the lateral hypothalamus on behavior and hippocampal and neocortical electroencephalographic (EEG) activity in the rat

Electrolytic lesions of the lateral hypothalamus (LH) are known to produce severe and chronic behavioral and electrographic abnormalities. In order to assess the effects of damage to LH cells vs damage to fibers of passage in the LH, a comparison was made of the effects of electrolytic lesions and micro-injections of the neurotoxin kainic acid (kainate) in the LH. Behavior and neocortical and hippocampal electroencephalographic (EEG) activity were studied before, immediately after, and for 25 days after the lesions were made. Electrolytic-lesioned rats were aphagic and adipsic, showed an absence of normal atropine-resistant EEG activity, and a release of atropine-sensitive EEG activity in the hippocampus and neocortex. Kainic acid-lesioned rats showed some similar behavioral impairments but the kainate lesions produced different EEG abnormalities, including chronic slow-wave and seizure activity in both the neocortex and hippocampus. Following extended recovery hippocampal EEG was normal despite extensive cellular loss in areas CA3 and CA4. Understanding of the differences in EEG between the electrolytic and kainate effects was compounded by widespread cellular damage in areas outside the hypothalamus in the rats with kainate lesions. Thus, the kainate-produced abnormalities precluded a simple analysis of the contribution that cell damage alone makes to LH lesion-induced behavioral and EEG changes.     

The postures of catecholamine-depletion catalepsy: their possible adaptive value in thermoregulation

Our view of the cataleptic akinesia induced by the disruption of catecholaminergic systems is that it is a state in which the postural and motor subsystems organized to maintain static stable equilibrium (e.g., standing or bracing, and righting) are functioning, whereas other subsystems such as those involved in exploration (walking, scanning, or orienting) and eating are inoperative. In addition to their role in actively maintaining stable equilibrium, the postures of cataleptic akinesia appear also to be related to thermoregulation. Slight skin warming in animals made cataleptic and akinetic following lateral hypothalamic lesions or intraventricular 6-hydroxydopamine causes a dramatic inactivation of tonic support (the subsystem involved in standing and bracing) and the animal subsides into a prone position. So profound is the torpor induced by warming that if the animal is slowly rolled over onto its back, it no longer rights itself. Furthermore, otherwise untreated normal rats made severely hypothermic by a period of immersion in cold water assume the crouched immobile postures of cataleptic akinesia seen in the uncooled, normothermic catecholamine-depleted animal. After a few minutes, shivering is superimposed on these postures. We suggest that the seemingly bizarre condition of cataleptic-akinesia can be viewed as a very simplified neural state organized to permit not only the regulation of stable equilibrium, but also shivering thermogenesis.