Is it possible to transfer learned coordination of head and forepaw movements in dogs

Dogs were trained for tonic forelimb flexion fixed to a lever in order to hold a cup with meat during eating, when the head was bent down to a foodwell. Before learning, the forelimb flexion is accompanied by the anticipatory lifting of the head bent down to the foodwell; following lowering of the head leads to an extension of the flexed forelimb. Simultaneous holding of the flexed forelimb and lowered head is achieved by learning. During the original learning, the innate head-forelimb coordination was rearranged into the opposite one. After the initial instrumental learning, the "working" forelimb was changed to test whether a transfer of the learned head-forelimb coordination would occur. It was shown that the execution of the instrumental reaction by the untrained forelimb was impossible, because the innate coordination between the head and this forelimb persisted. It could also be rearranged by learning. The involvement of the motor cortex in the unilateral rearrangement of the innate head-forelimb movement coordination is discussed.     

The role of the motor cortex in rearrangement of the innate movement coordination in the dog

In chronical experiments in dogs the pattern of shoulder muscle recruitment was examined during the forelimb flexion by which the animal lifted and held a cup of food during eating. At the early stage of the instrumental reaction learning the forelimb lifting was performed with the anticipatory deviation of the head in up direction, when the head bent down to the foodwell the lifted forelimb lowered. Simultaneous holding of the flexed forelimb and lowered head providing food reinforcement was achieved only by learning. It was found that the forelimb lifting in the innate coordination in untrained dogs was performed with activation of m. deltoideus and m. teres major, whereas m. teres minor was active whilst the dog was standing but the muscle activity was abolished before the limb lifting. In the course of learning m. teres minor activity was changed into opposite one. In the learned coordination the limb lifting was accompanied by the activation of all three shoulder flexors. The lesion of the motor cortex in the area of the "working" forelimb, but not in other areas led to disturbance of the learned coordination and the novel pattern of the shoulder muscle activity. The data obtained led to the following conclusion: the rearrangement of the innate coordination is connected with the formation of the novel way of the forelimb lifting which pattern of muscle recruitment is provided by the motor cortex.     

Cholinoceptive pontine reticular structures modify the postural adjustments during the limb movements induced by cortical stimulation

1. Activation of the pontine reticular formation (pRF) and the related medullary inhibitory reticulospinal (RS) system decreases the postural activity. This effect can be achieved either by local injection into the dorsal pontine tegmentum of cholinergic agonists which excite cholinoceptive pRF neurons, or by injection of noradrenergic agents which block the inhibitory influence exerted by the locus coeruleus (LC) neurons on the pRF. The main aim on the present study was to analyze the effects of tonic activation of these pRF neurons on the postural adjustments accompanying limb movements induced by motor cortex stimulation. In particular, electrodes were implanted chronically in the motor cortex of cats and stainless steel guide tubes of small size, later used for drug injection, were set bilaterally into sites just above the responsive regions. 2. Limb flexion elicited by stimulation of the motor cortex was accompanied by a diagonal pattern of postural adjustment, characterized by a decreased force exerted by the limb diagonally opposite to the moving one and an increased force exerted by the other two. 3. Microinjection into the pRF of both sides of 0.25 microliter of the muscarinic agonist bethanechol at the concentration of 8 or 16 micrograms/microliters in buffered artificial cerebrospinal fluid produced a short-lasting episode of postural atonia followed by a period of reduced postural activity, during which the cats were still able to stand on the measurement platform. Under this condition no changes in threshold, latency and amplitude of the flexion response were observed in the performing limb; however, the postural responses were considerably affected. In particular, when the performing limb was a forelimb, the other anterior limb showed a dissociation of the postural response in two distinct components. The first anticipatory component, which had a short latency (12-15 msec) and was considered to be centrally triggered, decreased in amplitude after injection of bethanechol and sometimes disappeared; on the other hand the second component, which had a long latency (50-60 msec) and was thus considered to be of reflex origin, increased in amplitude, due to the instability resulting from the depression of the early postural response. Similar results also affected to a lesser extent the hindlimbs. Moreover, body oscillations were observed and monitored from the force platforms following the late component of the postural responses.(ABSTRACT TRUNCATED AT 400 WORDS)     

Role of different projection areas of the motor cortex in reorganization of the innate head-forelimb coordination in dogs

Dogs were trained to perform the forelimb tonic flexion in order to lift a cup with meat from a bottom of the foodwell and hold it during eating with the head bent down to the cup. It is known that conditioning of the instrumental reaction is based on reorganization of the innate head-forelimb coordination into the opposite one. In untrained dogs, the forelimb flexion is accompanied by the anticipatory lifting of the head bent down to the foodwell. The following lowering of the head leads to an extension of the flexed forelimb. Tonic forelimb flexion is possible if the head is in the up position. Simultaneous holding of the flexed forelimb and lowered head providing food reinforcement is achieved only by learning. It was shown earlier that the lesion of the motor cortex contralateral to the "working" forelimb led to a prolonged disturbance of the elaborated coordination and reappearance of the innate coordination. In the present work we studied the influence of local lesions of the projection areas in the motor cortex, such as a "working" forelimb area, bilateral representation of the neck, and the medial part of the motor cortex, on the learned instrumental feeding reaction. It was found that only the lesion of the forelimb but not neck projection led to a disturbance of the learned head-forelimb movement coordination.     

Natural head-forelimb coordination in dogs after vestibular de-afferentation

We studied the influence of the vestibular lesion on the natural head--forelimb coordination. This coordination exists in intact dogs at the early stage of acquisition of the instrumental feeding reaction of tonic forelimb flexion in order to hold a cup with meat during eating when the head is bent down to foodwell. In untrained dogs, the forelimb flexion is preceded by lifting the head bent down to the food; the following lowering of the head leads to extension of the flexed forelimb. For performing the instrumental reaction, the innate coordination has to be rearranged into the opposite one. It is achieved only by learning. After the lesion of the primary motor cortex contralateral to the "working" forelimb in trained dogs, the innate coordination reappears, whereas the learned coordination breaks down steadily. It was shown that bilateral vestibular lesion do not disturb the innate coordination in intact dogs at the early stage of learning and in trained dogs after the motor cortex lesion. It was concluded that the studied natural head--forelimb coordination is not connected with the vestibular reflex.     

The participation of the cholinergic system of the rat sensorimotor cortex in regulating different types of movements

To study the role of the cholinergic system of the sensorimotor cortex in regulation of different manipulatory movements and locomotion of Wistar rats, the effects of injections of cholinergic drugs (a cholinergic agonist carbachol and an antagonist scopolamine) into the area of forepaw representation in the sensorimotor cortex on motor activity and performance of manipulatory movements (with prolonged and short pushing) were analyzed. The drugs were injected via special cannulae stereotaxically implanted into the cortex during surgery carried out under Nembutal anesthesia. Carbachol injections (0.03-3 micrograms in 1 microliter of physiologic solution) into the cortex resulted in a significant slowing down of both types of movements as well as an increase in locomotion in the open-field test. Injections of scopolamine (0.3-3 micrograms) into the same cortical area were accompanied by an increase in the number of fast manipulatory movements without significant changes in locomotor activity. The obtained evidence suggests that the cholinergic system of the sensorimotor cortex indifferent manners regulates the innate (locomotion) and acquired movements which require different periods of maintaining the muscle tone of the forepaw (short-time periods for the usual movements necessary for food taking from the narrow horizontal tube and prolonged periods for the learned slow movements with additional tactile and tonic components).     

Unitary activity in the cat motor cortex during a conditioned postural adjustment reflex

Unitary activity in the motor cortex (area 4) during a conditioned postural adjustment reflex was investigated in cats. Responses of the overwhelming majority of neurons connected with conditioned-reflex placing movements were activational in type. They consisted of several components and preceded the movements themselves by 50–600 msec. During realization of incorrect responses to presentation of a differential stimulus and of "spontaneous" interstimulus movements, the unitary responses were similar in direction but differed in their lower intensity and, in most cases, they appeared simultaneously with these movements. In the course of extinction both the conditioned-reflex movements and the corresponding unitary responses disappeared simultaneously. The technique of formation of a conditioned postural adjustment reflex suggested in this paper can be used to from natural, well-coordinated forelimb movements in animals in response to conditioned stimulation which are necessary initial components of more complex behavioral motor responses.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 745–753, November–December, 1984.     

Disruption of acquired head and paw movement coordination after unilateral lesioning of the motor cortex in dogs (a kinematic analysis)

Dogs were trained to remove a cup with meat to the head bent down to the feeder and hold the limb flexed during eating. At the early stage of learning, the stable innate head-forelimb coordination characteristic for untrained animals was manifest. The forelimb flexion was accompanied by anticipatory lifting of the bent head, and the following bending of the head led to an extension of the flexed forelimb. The opposite coordination, i.e., the lifting and holding of the forelimb when the head is bent down, was achieved only by training. The lesion of the motor cortex contralateral to the working forelimb in the trained dogs led to a prolonged disturbance of the simultaneous holding of the flexed forelimb and the head bent down. The lesion of the motor cortex did not affect the individual movements but disturbed their coordination. In the operated dogs the innate relationships between the head and forelimb movement recovered. The results support the previous finding that the lesion of the motor cortex led to recovery of the innate coordination transformed in the process of learning.     

Role of the motor area of the cortex in the performance of the postural escape reaction

It has been shown on three dogs that unilateral ablation of the cortical motor area temporally disturbs previously acquired and opposite to the innate postural escape reaction to electric stimulation of the contralateral forepaw by increasing its pressure on the support. After 3-4 months of repeated training, compensation is possible. Bilateral ablation of the motor cortex elicits stable and unreversible disturbance of the acquired reaction. In reorganization of postural coordinations, motor cortex functions are connected with the inhibition of innate coordinations preventing performance of the reaction.     

Role of the motor cortex in the control of axial and proximal muscles in learning

Involvement of the motor cortex in the control of the shoulder and the scapula muscles was studied during acquisition of the novel head-forelimb coordination in dogs. The dogs were trained to raise the forelimb fixed to the lever in order to lift a food-containing cup and keep it elevated during eating with the head tilted down to the feeder. At the early stage of learning, the movement of raising the limb occurred with an anticipatory upward head tilt, whereas the head tilt to the feeder was associated with the lowering of the raised limb. Food consumption required a new coordination, i.e., maintaining the raised limb in a posture with the head lowered. This coordination could only be achieved by learning. This new coordination was critically dependent on the intact motor cortex. It was found that in the natural coordination, raise of the limb involved regular activation of the main flexors of shoulder, i.e., deltoid and teres major muscles, and inconstant participation of teres minor, supra- and infraspinatus, trapezius muscles. Muscles of the latter group were often active during standing but ceased their activity before limb raise. The learned limb raise with the head tilted down occurred with activation of all the mentioned muscles, and some of them changed their activity for the opposite pattern. Lesions in the motor cortex (inclusive the main part of the projection area of the "working" limb) led to a restoration of the natural head-fore- limb coordination and the innate muscle pattern of the limb raise. Thus, in the course of learning, the motor cortex rearranges the innate pattern of coordination of phylogenetically old axial and proximal muscles, which begin to work in a new manner.     

Changes in electrical thresholds for evoking movements from the cat cerebral cortex following lesions of the sensori-motor area

We evaluated motor maps in the cerebral cortex and motor performance in cats before and after lesions of the forelimb representation in the primary motor area. After the lesion there was a reduction in the use of the affected forelimb and loss of accuracy in prehension tasks using the forelimb; some recovery occurred during the mapping study. Electrode tracts and lesion sites were located in cytoarchitectonically identified cortical areas 4γ, 4δ, 6aα, 6aγ, 3a. The lesions were mainly in area 4γ. In the lesioned hemisphere there were many points around the lesion site (in areas 4γ and 3a) from which movements could not be evoked. In some areas distant from the lesion site (e.g. area 6aγ) the mean thresholds for evoking forelimb movements were significantly elevated. Mean thresholds for evoking hindlimb and facial movements were not different from before. In the contralateral hemisphere mean thresholds for evoking forelimb, but not hindlimb or facial movements, were significantly elevated in several sensorimotor areas (area 4γ, 6aγ and 3a). Mean thresholds for evoking forelimb movements appeared to progressively increase during the time of study. Minimal currents required to evoke forelimb movements from the cerebral cortex increase (possibly progressively) following a lesion of the forelimb representation in the primary motor area, affecting many interconnected motor areas in the hemispheres ipsilateral and contralateral to the lesioned site. This increase in thresholds may play a role in the changes in cortical control of the affected and contralateral limbs following brain lesions and explain the increased sense of effort required to produce movements.     

Changes in electrical thresholds for evoking movements from the cat cerebral cortex following lesions of the sensori-motor area

We evaluated motor maps in the cerebral cortex and motor performance in cats before and after lesions of the forelimb representation in the primary motor area. After the lesion there was a reduction in the use of the affected forelimb and loss of accuracy in prehension tasks using the forelimb; some recovery occurred during the mapping study. Electrode tracts and lesion sites were located in cytoarchitectonically identified cortical areas 4gamma, 4delta, 6aalpha, 6agamma, 3a. The lesions were mainly in area 4gamma. In the lesioned hemisphere there were many points around the lesion site (in areas 4gamma and 3a) from which movements could not be evoked. In some areas distant from the lesion site (e.g. area 6agamma) the mean thresholds for evoking forelimb movements were significantly elevated. Mean thresholds for evoking hindlimb and facial movements were not different from before. In the contralateral hemisphere mean thresholds for evoking forelimb, but not hindlimb or facial movements, were significantly elevated in several sensorimotor areas (area 4gamma, 6agamma and 3a). Mean thresholds for evoking forelimb movements appeared to progressively increase during the time of study. Minimal currents required to evoke forelimb movements from the cerebral cortex increase (possibly progressively) following a lesion of the forelimb representation in the primary motor area, affecting many interconnected motor areas in the hemispheres ipsilateral and contralateral to the lesioned site. This increase in thresholds may play a role in the changes in cortical control of the affected and contralateral limbs following brain lesions and explain the increased sense of effort required to produce movements.     

Paw-Dragging: a Novel,Sensitive Analysis of the Mouse Cylinder Test

The cylinder test is routinely used to predict focal ischemic damage to the forelimb motor cortex in rodents. When placed in the cylinder, rodents explore by rearing and touching the walls of the cylinder with their forelimb paws for postural support. Following ischemic injury to the forelimb sensorimotor cortex, rats rely more heavily on their unaffected forelimb paw for postural support resulting in fewer touches with their affected paw which is termed forelimb asymmetry. In contrast, focal ischemic damage in the mouse brain fails to result in comparable consistent deficits in forelimb asymmetry. While forelimb asymmetry deficits are infrequently observed, mice do demonstrate a novel behaviour post stroke termed “paw-dragging”. Paw-dragging is the tendency for a mouse to drag its affected paw along the cylinder wall rather than directly push off from the wall when dismounting from a rear to a four-legged stance. We have previously demonstrated that paw-dragging behaviour is highly sensitive to small cortical ischemic injuries to the forelimb motor cortex. Here we provide a detailed protocol for paw-dragging analysis. We define what a paw-drag is and demonstrate how to quantify paw-dragging behaviour. The cylinder test is a simple and inexpensive test to administer and does not require pre-training or food deprivation strategies. In using paw-dragging analysis with the cylinder test, it fills a niche for predicting cortical ischemic injuries such as photothrombosis and Endothelin-1 (ET-1)-induced ischemia – two models that are ever-increasing in popularity and produce smaller focal injuries than middle cerebral artery occlusion. Finally, measuring paw-dragging behaviour in the cylinder test will allow studies of functional recovery after cortical injury using a wide cohort of transgenic mouse strains where previous forelimb asymmetry analysis has failed to detect consistent deficits.     

Presurgical functional localization of primary somatosensory cortex by dipole tracing method of scalp-skull-brain head model applied to somatosensory evoked potential

The aim of the present study was to explore the utility of dipole tracing (DT) of a scalp-skull-brain (SSB) head model in preoperative functional localization of the human brain. Nine patients who underwent surgery of mass lesions around the central sulcus (CS) were employed. By using SSB/DT, dipole source location of early cortical components of the somatosensory evoked potential (SEP) was estimated before surgery. Motor cortex, CS and primary somatosensory cortex were determined by cortical SEP during surgery. After surgery precise functional mapping was reproduced in MRI, and the accuracy of DT was evaluated by measuring the distance between estimated dipole source and the posterior bank of the CS. We defined this distance as localization error of DT. In 4 cases without structural change around the sensorimotor cortex, localization error ranged from 1 to 4 mm with an average of 2 mm. In 5 cases with structural alteration of sensorimotor cortex, localization error ranged from 6 to 10 mm with an average of 8 mm. The difference in localization error between the two groups was statistically significant, and may have been caused by changes of conductance near sensorimotor cortex in the latter group. Functional localization by DT was accurate and useful. But localization error could not be ignored in cases with structural alteration in the sensorimotor cortex.     

Participation of the motor cortex in the bimanual unloading task: a study by transcranial magnetic stimulation

Motor potentials of m. biceps brachii evoked by transcranial magnetic stimulation of the contralateral motor cortex have been recorded in postural adjustment during arm unloading in humans. During active unloading, the amplitude of the motor evoked potential decreases simultaneously with the decreasing of the muscle activity. During load keeping, the muscle response changes simultaneously with the load changes. When the other arm has lifted the other load during load keeping, the amplitude of the motor evoked potential decreases in the m. biceps of the keeping arm without muscle activity changes. Passive unloading results in the same changes of the motor evoked potential as active unloading. A possible role of the direct corticospinal volley and the motor command mediated by some subcortical structures in the decrease of the muscle activity preceding active unloading (postural adjustment) is discussed.     

Anticipatory postural adjustment in bimanual unloading: role of the motor cortex in motor learning

The role of the motor cortex was investigated during learning unusual postural adjustment. Healthy subjects held their right (postural) forearm in a horizontal position while supporting a 1-kG load via an electromagnet. The postural forearm position was perturbed by the load release triggered by other elbow voluntary movement. Repetition of the imposed unloading test resulted in a progressive reduction of the maximal forearm rotation, accompanied by the anticipatory decrease in m. biceps brachii activity (learning). Control situation consisted of the voluntary forearm loading. Using the transcranial magnetic stimulation we examined changes in the motor evoked potential of the m. biceps brahii at the beginning and at the end of learning. The evoked potential amplitude did not significantly change in process of the decrease of m. biceps brachii activity. At the end of learning, motor evoked potential / baseline electromyogram ratio increased as compared to the beginning of learning and to the control situation. The results highlight the fundamental role of the motor cortex in suppression of synergies which interfere with formation of a new coordination during motor learning.     

Sensorimotor experience influences recovery of forelimb abilities but not tissue loss after focal cortical compression in adult rats

Sensorimotor activity has been shown to play a key role in functional outcome after extensive brain damage. This study was aimed at assessing the influence of sensorimotor experience through subject-environment interactions on the time course of both lesion and gliosis volumes as well as on the recovery of forelimb sensorimotor abilities following focal cortical injury. The lesion consisted of a cortical compression targeting the forepaw representational area within the primary somatosensory cortex of adult rats. After the cortical lesion, rats were randomly subjected to various postlesion conditions: unilateral C5-C6 dorsal root transection depriving the contralateral cortex from forepaw somatosensory inputs, standard housing or an enriched environment promoting sensorimotor experience and social interactions. Behavioral tests were used to assess forelimb placement during locomotion, forelimb-use asymmetry, and forepaw tactile sensitivity. For each group, the time course of tissue loss was described and the gliosis volume over the first postoperative month was evaluated using an unbiased stereological method. Consistent with previous studies, recovery of behavioral abilities was found to depend on post-injury experience. Indeed, increased sensorimotor activity initiated early in an enriched environment induced a rapid and more complete behavioral recovery compared with standard housing. In contrast, severe deprivation of peripheral sensory inputs led to a delayed and only partial sensorimotor recovery. The dorsal rhizotomy was found to increase the perilesional gliosis in comparison to standard or enriched environments. These findings provide further evidence that early sensory experience has a beneficial influence on the onset and time course of functional recovery after focal brain injury.     

Functionally specific reorganization in human premotor cortex

After unilateral stroke, the dorsal premotor cortex (PMd) in the intact hemisphere is often more active during movement of an affected limb. Whether this contributes to motor recovery is unclear. Functional magnetic resonance imaging (fMRI) was used to investigate short-term reorganization in right PMd after transcranial magnetic stimulation (TMS) disrupted the dominant left PMd, which is specialized for action selection. Even when 1 Hz left PMd TMS had no effect on behavior, there was a compensatory increase in activity in right PMd and connected medial premotor areas. This activity was specific to task periods of action selection as opposed to action execution. Compensatory activation changes were both functionally specific and anatomically specific: the same pattern was not seen after TMS of left sensorimotor cortex. Subsequent TMS of the reorganized right PMd did disrupt performance. Thus, this pattern of functional reorganization has a causal role in preserving behavior after neuronal challenge.     

Comparison of electrical thresholds for evoking movements from sensori-motor areas of the cat cerebral cortex and its relation to motor training

Motor maps and electrical thresholds for evoking movements from motor areas of the cerebral cortex were evaluated in normal cats by using intracortical microstimulation techniques. Stainless steel chambers were implanted over craniotomies in adult cats trained to perform reaching and retrieval movements with their forelimbs. Prehensile motor training was continued and movement performance monitored for about 6–10 weeks during which the cortex was progressively explored with sharp tungsten electrodes inserted into cortical gyri (anterior and posterior sigmoid, and coronal) and the banks of sulci (cruciate, presylvian and coronal). Twice weekly, under light general anaesthesia, 3–4 tracks were made in either hemisphere till about 50 tracks were made in each hemisphere. Mean thresholds for evoking forelimb movements from different cytoarchitectonic areas (4γ, 4δ, 6aγ and 3a) were compared and no consistent or significant differences were observed between the different areas. In the animals (4/6) which used either forelimb to perform the tasks, there were no consistent differences in the mean thresholds for evoking forelimb movements from the two hemispheres. However, in 2 animals, which used their right forelimbs predominantly or exclusively to perform all the tasks, mean thresholds for evoking forelimb movements was significantly higher in areas 4γ and 6aγ of the left hemisphere (compared to the right); no consistent differences in the mean thresholds for evoking hindlimb or facial movements were observed between the two hemispheres. These findings suggest that ICMS thresholds for evoking forelimb movements may be similar in different sensorimotor areas of the cat cerebral cortex, and these thresholds could be influenced by motor training.     

Comparison of electrical thresholds for evoking movements from sensori-motor areas of the cat cerebral cortex and its relation to motor training

Motor maps and electrical thresholds for evoking movements from motor areas of the cerebral cortex were evaluated in normal cats by using intracortical microstimulation techniques. Stainless steel chambers were implanted over craniotomies in adult cats trained to perform reaching and retrieval movements with their forelimbs. Prehensile motor training was continued and movement performance monitored for about 6-10 weeks during which the cortex was progressively explored with sharp tungsten electrodes inserted into cortical gyri (anterior and posterior sigmoid, and coronal) and the banks of sulci (cruciate, presylvian and coronal). Twice weekly, under light general anaesthesia, 3-4 tracks were made in either hemisphere till about 50 tracks were made in each hemisphere. Mean thresholds for evoking forelimb movements from different cytoarchitectonic areas (4gamma, 4delta, 6agamma and 3a) were compared and no consistent or significant differences were observed between the different areas. In the animals (4/6) which used either forelimb to perform the tasks, there were no consistent differences in the mean thresholds for evoking forelimb movements from the two hemispheres. However, in 2 animals, which used their right forelimbs predominantly or exclusively to perform all the tasks, mean thresholds for evoking forelimb movements was significantly higher in areas 4gamma and 6agamma of the left hemisphere (compared to the right); no consistent differences in the mean thresholds for evoking hindlimb or facial movements were observed between the two hemispheres. These findings suggest that ICMS thresholds for evoking forelimb movements may be similar in different sensorimotor areas of the cat cerebral cortex, and these thresholds could be influenced by motor training.