Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with "substitution" and "vicariation" (adaptive plasticity) models of recovery from brain damage and stroke.

Vestibular inputs tonically activate the anti-gravitative leg muscles during normal standing in humans, and visual information and proprioceptive inputs from the legs are very sensitive sensory loops for body sway control. This study investigated the postural control in a homogeneous population of 50 unilateral vestibular-deficient patients (Ménière's disease patients). It analyzed the postural deficits of the patients before and after surgical treatment (unilateral vestibular neurotomy) of their diseases and it focused on the visual contribution to the fine regulation of body sway. Static posturographic recordings on a stable force-plate were done with patients with eyes open (EO) and eyes closed (EC). Body sway and visual stabilization of posture were evaluated by computing sway area with and without vision and by calculating the percentage difference of sway between EC and EO conditions. Ménière's patients were examined when asymptomatic, 1 day before unilateral vestibular neurotomy, and during the time-course of recovery (1 week, 2 weeks, 1 month, 3 months, and 1 year). Data from the patients were compared with those recorded in 26 healthy, age- and sex-matched participants. Patients before neurotomy exhibited significantly greater sway area than controls with both EO (+52%) and EC (+93%). Healthy participants and Ménière's patients, however, displayed two different behaviors with EC. In both populations, 54% of the subjects significantly increased their body sway upon eye closure, whereas 46% exhibited no change or significantly swayed less without vision. This was statistically confirmed by the cluster analysis, which clearly split the controls and the patients into two well-identified subgroups, relying heavily on vision (visual strategy, V) or not (non-visual strategy, NV). The percentage difference of sway averaged +36.7%+/-10.9% and -6.2%+/-16.5% for the V and NV controls, respectively; +45.9%+/-16.8% and -4.2%+/-14.9% for the V and NV patients, respectively. These two distinct V and NV strategies seemed consistent over time in individual subjects. Body sway area was strongly increased in all patients with EO early after neurotomy (1 and 2 weeks) and regained preoperative values later on. In contrast, sway area as well as the percentage difference of sway were differently modified in the two subgroups of patients with EC during the early stage of recovery. The NV patients swayed more, whereas the V patients swayed less without vision. This surprising finding, indicating that patients switched strategies with respect to their preoperative behavior, was consistently observed in 45 out of the 50 Ménière's patients during the whole postoperative period, up to 1 year. We concluded that there is a differential weighting of visual inputs for the fine regulation of posture in both healthy participants and Ménière's patients before surgical treatment. This differential weighting was correlated neither with age or sex factors, nor with the clinical variables at our disposal in the patients. It can be accounted fo...

The representation of the surfaces of the trunk was mapped in detail in a series of anesthetized adult female rats to assess cortical representational changes that might be induced in the SI cortical field by a major natural source of a differentially heavy schedule of tactile inputs: the stimulation of the rat ventrum in nursing behavior. Controls included virgin rats and postpartum age-matched rats whose litters were removed on the day of birth. The SI representation of the ventral trunk skin of lactating rats was about 1.6 x larger than in matched postpartum nonlactating or virgin controls. The greatest representational change--about twofold--was for the nipple-bearing skin between the forelimbs and hindlimbs. Indeed, changes in SI representational territory for the middle third of the ventrum, a skin zone without nipples, were not significant. As a rule, the representation of the ventrum skin in lactating rats was at least as topographically ordered as was that reconstructed for nonlactating postpartum and virgin controls. Receptive fields (RFs) representing the ventrum skin in lactating females were about one-third the sizes of those recorded in matched nonlactating or virgin controls. RF size differences were again greater for the representation of the nipple- bearing skin in the anterior and posterior thirds of the ventrum than for the central third. Changes in RF sizes were roughly inversely related to changes in the cortical magnification of representation of the ventrum on the proportion of about 3:2. Interestingly, the glabrous nipple and areolar skin were only weakly represented--or not demonstrably represented--in the SI map of either lactating or control rats. These results indicate that there is a largely unstudied cortical neurology of nursing behavior. Major CNS changes are induced by this dramatic, episodic change in behaviorally important tactile inputs. In turn, input-induced changes presumably contribute to this emergent, rapidly evolving behavior.

The cortical forepaw area of young adult rats was mapped by recording the response properties of small clusters of neurons in layer IV of the primary somatosensory (SI) cortex. First we quantitatively analyzed the somatotopic organizational features of the cortical forepaw representation in terms of areal extent and topography, receptive field (RF) sensory modality, size, and location. We also assessed the influence of environmental enrichment, known to induce structural alterations in cortical connectivity, on the representational characteristics of the forepaw maps. Long-Evans rats were housed in environments (standard, SE; enriched, EE) promoting differential tactile experience for 71-113 days from weaning. Within the SI, we found a single and complete topographic map of the cutaneous surfaces of the forepaw consisting of a rostrolateral-caudomedial sequence of digit and pad representational zones. Small islets of noncutaneous responses (NCR; high-threshold, deep-receptor input) within the boundaries of the cutaneous maps were a conspicuous feature of the forepaw map for SE rats. These islets created discontinuities in the representation of contiguous skin territories. In the SE rats, about 79% of the cortical sites activated by light tactile stimulation had a single cutaneous RF, whereas about 21% exhibited multiple RFs. Most single-digit RFs we delineated in the SE rats extended across two or three phalanges. As a result, the representations of the phalangeal skin surfaces were not segregated but formed an overlapping continuum. Moreover, within these regions, as the electrode was displaced in regular steps across the mediolateral axis, RFs did not shift across the digit skin surface in an orderly manner, suggesting a lack of internal topography in the finger representation zones. Tactile experience promoted by environmental enrichment induced alterations in the representational features of the SI cutaneous map of the forepaw. In EE rats, the areal extent of the forepaw cutaneous representation was 1.5 times larger than in SE rats. Indeed, the cutaneous map extended into NCR cortical sectors along its external margins and also into NCR islets found in the forepaw area. Consequently, in EE rats there were fewer representational discontinuities. The areal enlargement was due to a selective increase in the areal extent of the glabrous but not the hairy skin surface representations. Furthermore, protuberant glabrous skin (digit tips, palmar pads) was represented over larger cortical regions than were other glabrous skin territories less likely to be stimulated during object palpation and manipulation. Maps from EE rats were also characterized by a larger proportion of sites with single RFs (88% compared with 79%). In addition, glabrous RFs from EE rats were smaller and more clustered on the digit tips and palmar pads than were RFs in SE rat maps. RF size on hairy skin surfaces remained unchanged. Because the RFs were smaller, the cutaneous maps of EE rats contained distinct representations of digit phalangeal gl...

The representations of the surfaces of the hand in the primary somatosensory cortical field, area 3b, were reconstructed in detail in seven owl monkeys and two squirrel monkeys trained to pick up food pellets from five wells of different sizes. From an early clumsy performance in which several to many retrieval attempts were required for each successful pellet retrieval, the monkeys exhibited a gradual improvement in digital dexterity as shown by significant decreases in mean numbers of grasp attempts/successful retrieval and corresponding standard deviations (e.g. 5.8 ± 4.5 and 4.8 ± 3.1 respectively, for the smallest well) between the first and last training sessions. All monkeys commonly used alternative, specific retrieval strategies involving various combinations of digits for significant time epochs before developing a highly successful strategy, which, once achieved, was rapidly stereotyped. For example, the numbers of digit combinations used during the first five versus the last five training sessions decreased from 3.3 ± 0.7 to 1.8 ± 0.6 for the smallest well. In both owl and squirrel monkeys, as the behavior came to be stereotyped, monkeys reliably engaged limited surfaces of the glabrous tips of two digits (in eight monkeys), or of three digits (in one monkey) in the palpation and manipulation of these small pellets for their location, capture, and transportation to the mouth. In cortical area 3b, the magnification of representation of these differentially engaged glabrous fingertip surfaces was nearly 2× larger than for the corresponding surfaces of other hand digits, or for the contralateral cortical representations of the same digit surfaces on the opposite hand. In parallel, cutaneous receptive field for area 3b neurons representing crucial digital tip surfaces were less than half as large as were those representing the corresponding surfaces of control digits. Receptive field overlaps were smaller on the trained fingertips than on control fingers. Moreover, the proportion of small overlaps was greater for the trained digits (76 ± 7%) than for the other digits of the same hand (49 ± 5.4%). There was still a simple, single -but apparently topologically expanded -representation of these differentially engaged skin surfaces in these monkeys. Thus, with very limited manual exercise over a total period of a few hours of practice at a skill played out in brief daily sessions over a several week long training period, the representations of skin surfaces providing information crucial for successfully performing a small-object retrieval behavior appeared to be substantially remodeled in the most 'primary' of the SI somatosensory cortical fields, cortical area 3b. By that remodeling, behaviorally important skin surfaces were represented in a much finer representational grain than normal. Some implications of these findings for motor skill acquisition are discussed. IntroductionIn earlier studies, we have shown that the details of the cortical representations of the hand surfaces in adult monkeys are modifie...

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