Interplay between intra- and interhemispheric remodeling of neural networks as a substrate of functional recovery after stroke: adaptive versus maladaptive reorganization.

Brain injuries such as focal stroke initiate a myriad of neural events leading to local and remote alterations in cerebral networks. The neurochemical and neurophysiological mechanisms underlying these postlesion changes raise the question of their beneficial or adverse effects on functional recovery. In this review, we aim to reconcile findings from animal and patients studies using a "from cellular-to network-levels" perspective to gain further insights into the neuroplasticity mechanisms underlying recovery of sensorimotor functions. Ultimately, an integrative view of the multiple facets of poststroke changes should give an impetus to novel neurorehabilitation strategies by providing evidence of how neuroscience findings can be translated and operationalized within the context of restorative stroke.

Neuronal substrates of haptic shape encoding and matching: a functional magnetic resonance imaging study.

We used functional magnetic resonance imaging to differentiate cerebral areas involved in two different dimensions of haptic shape perception: encoding and matching. For this purpose, healthy right-handed subjects were asked to compare pairs of complex 2D geometrical tactile shapes presented in a sequential two-alternative forced-choice task. Shape encoding involved a large sensorimotor network including the primary (SI) and secondary (SII) somatosensory cortex, the anterior part of the intraparietal sulcus (IPA) and of the supramarginal gyrus (SMG), regions previously associated with somatosensory shape perception. Activations were also observed in posterior parietal regions (aSPL), motor and premotor regions (primary motor cortex (MI), ventral premotor cortex, dorsal premotor cortex, supplementary motor area), as well as prefrontal areas (aPFC, VLPFC), parietal-occipital cortex (POC) and cerebellum. We propose that this distributed network reflects construction and maintenance of sensorimotor traces of exploration hand movements during complex shape encoding, and subsequent transformation of these traces into a more abstract shape representation using kinesthetic imagery. Moreover, haptic shape encoding was found to activate the left lateral occipital complex (LOC), thus corroborating the implication of this extrastriate visual area in multisensory shape representation, besides its contribution to visual imagery. Furthermore, left hemisphere predominance was shown during encoding, whereas right hemisphere predominance was associated with the matching process. Activations of SI, MI, PMd and aSPL, which were predominant in the left hemisphere during the encoding, were shifted to the right hemisphere during the matching. In addition, new activations emerged (right dorsolateral pre-frontal cortex, bilateral inferior parietal lobe, right SII) suggesting their specific involvement during 2D geometrical shape matching.

Deficits and recovery of body stabilization during acrobatic locomotion after focal lesion to the somatosensory cortex: a kinematic analysis combined with cortical mapping.

We used a kinematic analysis for assessing locomotor impairments and evaluating the time course of recovery after focal injury to the forepaw area of the primary somatosensory cortex (SI) in rats. The animals were trained to traverse a beam that was rotated at various speeds. Changes in orientation of the body and independent movement of the anterior and posterior parts of the body were reconstructed using a 3D motion analysis. In addition, we used electrophysiological cortical mapping to search for neurophysiological changes within the spared cortical zones surrounding the lesion. Neuronal recordings were performed in the same animals prior to and 3 weeks after the lesion induction. Our findings show that a focal lesion that destroyed about 60% of the forepaw representational zone was sufficient to cause conspicuous impairments in the rats' ability to produce adequate motor adjustments to compensate for the lateral shift of the beam and to avoid falling. The main deficits were reflected in a lack of appropriate coordination between the anterior and posterior parts of the body and an inability to maintain a regular gait during locomotion. Skilled locomotion was fully recovered within a 2-3 week period. Functional recovery cannot be ascribed to a restitution of the lost sensory representations. A permanent decrease of forepaw representation was recorded despite the re-emergence of restricted representational sectors in the peri-lesion zone. We suggest that alterations may have occurred in other cortical and subcortical areas interconnected with the injured area. It is also conceivable that the functional recovery involved an increased reliance on all the available sources of sensorimotor regulation as well as the use of behavioral strategies.

Influence of the postlesion environment and chronic piracetam treatment on the organization of the somatotopic map in the rat primary somatosensory cortex after focal cortical injury.

The influence of housing in an enriched or impoverished environment and anti-ischemic treatment (piracetam) on the organization of the intact regions of the somatosensory cortical maps adjacent to a focal cortical injury were investigated in adult rats. Response properties of small clusters of neurons were recorded in the area of the primary somatosensory cortex (SI) devoted to the contralateral forepaw representation. Electrophysiological maps were elaborated on the basis of the sensory "submodality" (cutaneous or noncutaneous) and the location of the receptive fields (RFs) of layer IV neurons. Recordings were made before, and 3 weeks after induction of a focal neurovascular lesion to the SI cortex. The main results were: 1) the focal ischemic injury induced a cellular loss which was less severe in the piracetam treated rats, regardless of the housing conditions; 2) the lesion resulted in a compression of the remaining forepaw map, a fragmentation of the representational zones serving the cutaneous surfaces (low-threshold inputs) and an enlargement of noncutaneous zones (high-threshold inputs) in the spared cortical sectors surrounding the lesion. These changes were found in all placebo rats, with the most detrimental effects in the animals exposed to an impoverished environment, and in the piracetam-plus-impoverished rats. In contrast, a limited compression of the forepaw map and a preservation of most representational sectors were observed in the piracetam-plus-enriched animals, 3) the size of the cutaneous RFs of the neurons within the intact cortical zones remained unchanged, regardless of environment or treatment; 4) consistent with the map changes, the skin surfaces lacking low-threshold cutaneous RFs increased after the lesion in all animal groups but the piracetam-plus-enriched rats; 5) cortical responsiveness as assessed with mechanical threshold evaluation was diminished in the placebo rats, whatever the environment, and in the piracetam-impoverished rats, but was not significantly affected in the piracetam-enriched animals. Our findings, based on the first double electrophysiological mapping in the rat SI cortex, highlight the protective effects of an environmental therapy associated with an anti-ischemic treatment on the neurophysiological properties of cortical neurons following a focal neurovascular injury to the neocortex.

Neuroprotective effects on somatotopic maps resulting from piracetam treatment and environmental enrichment after focal cortical injury.

Acute and chronic postlesion reorganization of the cortical maps was examined in adult rats using electrophysiological mapping of the forepaw area in the primary somatosensory cortex. Recordings were made before and after (first 12 hr and 3 wk) induction of a focal thermal-ischemic lesion to a restricted part of the forepaw area. The influence of an anti-ischemic substance (piracetam) and housing in an enriched environment (EE) or impoverished environment (IE) on the organization of the spared regions of the cortical maps adjacent to the lesion was investigated. The results revealed (1) a gradual expansion of the injured zone and a cellular loss that were smaller in the piracetam-treated (PT) rats than in the placebo (PL) rats; (2) a better preservation of the somatotopic organization and the neuronal responsiveness in the maps of the PT rats during the first 12 hr after the lesion; (3) a gradual compression and fragmentation of the remaining forepaw map over the first 3 postlesion wk. These changes were found in all PL rats, with the most detrimental effects in the animals exposed to an IE. In the PT-EE animals, a contrasting substantial preservation of the map was observed. (4) Cortical responsiveness was diminished in the PL rats, whatever the environment, and in the PT-IE rats; but it was not significantly affected in the PT-EE animals. The findings demonstrate the protective function of acute piracetam treatment on electrophysiological properties of cortical neurons within the peri-infarct tissue and highlight the neuroprotective effects of an environmental therapy combined with the piracetam treatment during the weeks after ischemic damage.

Sensorimotor experience modulates age-dependent alterations of the forepaw representation in the rat primary somatosensory cortex.

In a previous study, we found that the forepaw representation in the primary somatosensory cortex of rats housed in standard laboratory conditions was drastically altered during the aging process. In other studies we reported that exposure to an enriched environment improved the topographical organization and increased the spatial resolution of the forepaw cutaneous map in young adult rats, whereas housing in impoverished environment resulted in a loss of somatotopic details in the forepaw map. The main purpose of the present study was to investigate the influence of differential sensorimotor experience promoted by exposure to enriched or impoverished environments on the mutability of the cortical forepaw representation during aging. Two groups of Long-Evans rats were reared in enriched and impoverished environments from weaning to the age of 3.5-5 months (young adults), 6.5-8 months (mature rats), and 23-28 months (senescent rats). The electrophysiological maps of the forepaw representation were based on the somatosensory 'submodality' (cutaneous vs. non-cutaneous), size, and location of the receptive fields of small clusters of layer IV neurons. Moreover, the mechanical thresholds of neuronal response to cutaneous stimulation were assessed with calibrated von Frey filaments in mature and senescent animals. Age-related alterations of the topographic features of the forepaw map were characterized by a decrease in and a fragmentation of the cortical zones serving the glabrous skin of the forepaw. These changes were less pronounced in the enriched rats than in the impoverished rats. Glabrous skin receptive fields were smaller in young adult and mature enriched rats than in their impoverished counterparts. However, during aging glabrous receptive fields increased in the enriched rats, but decreased in the senescent impoverished rats so that old rats of either groups displayed receptive fields of similar sizes; in contrast, the size of hairy skin receptive fields was not affected by housing conditions or aging. Measurement of the neuronal responses to calibrated forces applied to the skin indicated that cortical excitability to near-threshold cutaneous input was lower in senescent rats than in mature rats, regardless of environmental conditions. The present study demonstrates that use-dependent remodeling of somatosensory maps occurs throughout life and that environmental and social interactions can partially offset the age-related breakdown of somatosensory cortical maps.

Age-related alteration of the forepaw representation in the rat primary somatosensory cortex.

The cortical forepaw representation of adult rats was mapped by using multiunit recordings of layer IV neurons within the primary somatosensory cortex. Electrophysiological maps were based on somatosensory "submodality" (cutaneous vs non-cutaneous), location and size of the receptive fields. Age-related changes in the organizational features of the forepaw representation in the primary somatosensory cortex were analysed in adult rats whose ages ranged from 3.5 to five months (young), about eight months (mature), 15-17months (presenescent) to 24-28months (senescent). Rats were housed from weaning (30days postnatal) in a standard laboratory environment. The organization of the forepaw map was not gradually altered with advancing age, but striking changes occurred in early adulthood (before eight months) and did not progress with further aging. The main alterations consisted of a prominent decrease in, and a fragmentation of, the cutaneous area of the forepaw representation. Representational zones formerly serving cutaneous surfaces became predominantly activated by high-threshold, presumably non-cutaneous, inputs which appeared somatotopically organized. These emergent non-cutaneous zones were interspersed with cutaneous sectors, thereby disrupting the somatotopic organization of the map of the forepaw skin. No significant modification in the size of glabrous or hairy cutaneous receptive fields accompanied these changes. Subjective evaluation of the responses evoked by tactile stimulation suggests that neuronal responsiveness was increased in the eight- to 17-month-old rats, but less so in the 24- to 28-month-old animals. These results indicate that degradation of the somatotopic organization of the cutaneous representation of the forepaw in the rat somatosensory cortex occurs early during the course of adult life.

Acute reorganization of the forepaw representation in the rat SI cortex after focal cortical injury: neuroprotective effects of piracetam treatment.

Immediate postlesion reorganization of the somatosensory cortical representation was examined in adult rats. Response properties of small clusters of neurons were recorded in the area of the primary somatosensory cortex (SI) devoted to the contralateral forepaw representation. Electrophysiological maps were elaborated on the basis of the sensory 'submodality' (cutaneous or noncutaneous) and the location of the peripheral receptive fields (RFs) of layer IV neurons. Recordings were made prior to, and from 1 to 12 h after, induction of a focal neurovascular lesion to the SI cortex that initially destroyed a part (8.5%) of the cutaneous representation. Moreover, the influence of an anti-ischaemic substance (piracetam) on lesion-induced changes was analysed. The main observations were: (i) a gradual outward expansion of the area of the functional lesion, which was smaller in the piracetam-treated (PT) rats than in the control, placebo-treated (PL) rats; (ii) a substantial remodelling of the spared representational zones, both in cortical sectors adjoining the site of injury and those remote from the site; (iii) a significant postlesion increase in the size of cutaneous RFs in the PT rats, but not in the PL rats; (iv) a better preservation of RF submodality and topographic organization in the PT maps than in the PL maps; and (v) a decrease in neuronal responsiveness to cutaneous stimulation which was less pronounced in the PT than in the PL rats. Our results can be ascribed to a rapid change in the balance of excitatory and inhibitory connections which leads to unmasking of subthreshold inputs converging onto cortical neurons. Our findings also indicate that acute piracetam treatment exerts a protective function on the physiological response properties of cortical neurons after focal injury.

Representational plasticity in cortical area 3b paralleling tactual-motor skill acquisition in adult monkeys.

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 2x 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.

Tactile impoverishment and sensorimotor restriction deteriorate the forepaw cutaneous map in the primary somatosensory cortex of adult rats.

We investigated the effects of sensory deprivation on the forepaw representation in the primary somatosensory cortex (SI) in the adult rat. Cortical maps were constructed from high-resolution multiunit recordings of the response of layer IV neurons to somatosensory stimuli. The main features of the forepaw representation were described in terms of areal extent and topography of the cortical map, and sensory submodality, size, and location of the receptive field (RF) of small clusters of the cortical neurons. After being weaned, two groups of Long-Evans rats were housed in a standard (SE) or impoverished (IE) environment for 65-115 days. A third group of SE rats was subjected to severe sensorimotor restriction (SR) of one forepaw for 7 days or 14 days, by using a one-sleeved cast. A concomitant effect of unilateral forelimb immobilization was a forced use of the nonrestricted forelimb in postural balance. The maps of both forepaws were derived 24 h after the cast was removed and the animal was allowed normal limb use. In a fourth group, SE rats experienced a 7-day immobilization followed by symmetrical limb use for 7 days before we mapped the hemisphere contralateral to the casted limb. For the SE and IE rats, the total areal extent of the cutaneous forepaw representation was similar, but IE rats exhibited a significant expansion of cortical islets serving high-threshold, presumably noncutaneous inputs, which were included in the cutaneous maps. In addition, SI neurons of IE rats had greatly enlarged glabrous, but not hairy, skin RFs. For the SR rats, the areal extent of the cutaneous map of the casted forepaw decreased by about 50%, after both 7- and 14-day forelimb immobilization. Large cortical sectors presumed to be formerly activated by cutaneous inputs were driven by high-threshold inputs that disrupted the somatotopic representation of the forepaw skin surfaces. These "emergent" representational sectors were topographically organized. By contrast, the areal extent and topography of the non-casted forepaw representation did not differ from those of SE rats. The size of glabrous RFs on the casted forepaw was similar to that of SE rats. On the contrary, glabrous RFs on the noncasted forepaw of SR rats were larger than those on their casted forepaw. The size of hairy RFs was not altered by the forelimb restriction. Interestingly, alteration of the somatotopic features of the casted forepaw map persisted after 7 days of symmetric use of the forelimbs. The present study demonstrates that continuous sensory experience is needed for the organizational features of SI maps to be maintained.

Environmental enrichment alters organizational features of the forepaw representation in the primary somatosensory cortex of adult rats.

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 glabrous skin. RFs tended to exhibit more orderliness in their progression across the digit glabrous skin of EE rats than they did in SE rats. The phalanges of EE rats were represented in distinct patches. Neurons in EE rats were more sensitive to light tactile stimulation than were neurons in SE rats. These alterations were presumably mediated by the selective potentiation of cutaneous over deep-receptor activation. More generally, the present study corroborates the view that cortical cutaneous maps are maintained in a permanent state of use-dependent fluctuation.

Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys.

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.

Sensory strategies in human postural control before and after unilateral vestibular neurotomy.

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 for by a different selection of sensory orientation references depending on the personal experience of the subjects, leading to a more or less heavy dependence on vision. The change of sensory strategy in the patients who had undergone neurotomy might reflect a reweighting of the visual and somatosensory cues controlling balance. Switching strategy by means of a new sensory selection of orientation references may be a fast adaptive response to the lesion-induced postural instability.

Vestibular compensation: role of visual motion cues in the recovery of posturo-kinetic functions in the cat.

Vision has long been recognized as a sensorimotor system which plays a major role in substitution for functional deficits induced by unilateral or bilateral exclusion of primary vestibular afferents. Little is known, however, about the post-lesion influence of visual inputs on the recovery of posturo-kinetic balance in a situation where fine, well-coordinated locomotor adjustments are required. The present study was carried out in order to gain some insight into the role played by motion vision in the restoration of fine posturo-kinetic balance in adult cats subjected to unilateral vestibular neurectomy. Prior to the lesion, 15 adult animals were trained to cross a beam rotating at various speeds. Their best global balance performance (highest beam rotation speed that did not provoke falling) and their average locomotion speed were evaluated. After the lesion, the cats were separated into three groups: (1) five animals were placed in a normal environment (animal house) (NV cats); (2) four animals were exposed to stroboscopic illumination which eliminated visual motion cues (SV cats) for 2 weeks following the lesion; and (3) three animals were placed in a normal environment and their training was interrupted for the same period as in the SV cats (NVI cats). The possible influence of the 2-week deprivation of visual motion cues on posturo-kinetic balance was also examined in three intact cats. The present behavioral study showed that: (1) early sensory deprivation caused suspension of the posturo-kinetic balance recovery process as long as it was maintained; (2) complete restoration of global balance capacities developed following the vestibular neurectomy after a significant delay in half of the SV cats; (3) the lack of motion cues resulted in severe alterations of fine posturo-kinetic balance (inappropriate dynamic motor adjustments and irregular locomotion speed regulation) in all SV cats; and (4) the visual deprivation induced a 2-week delay in the restoration of fine locomotor balance. These findings provide evidence for a defect in the visual sensory substitution processes that normally take place within the first few weeks following exclusion of primary vestibular afferents.

Experience-induced plasticity of cutaneous maps in the primary somatosensory cortex of adult monkeys and rats.

In a first study, the representations of skin surfaces of the hand in the primary somatosensory cortex, area 3b, were reconstructed in owl monkeys and squirrel monkeys trained to pick up food pellets from small, shallow wells, a task which required skilled use of the digits. Training sessions included limited manual exercise over a total period of a few hours of practice. From an early clumsy performance in which many retrieval attempts were required for each successful pellet retrieval, the monkeys exhibited a gradual improvement. Typically, the animals used various combinations of digits before developing a successful retrieval strategy. As the behavior came to be stereotyped, monkeys consistently engaged surfaces of the distal phalanges of one or two digits in the palpation and capture of food pellets from the smallest wells. Microelectrode mapping of the hand surfaces revealed that the glabrous skin of the fingertips predominantly involved in the dexterity task was represented over topographically expanded cortical sectors. Furthermore, cutaneous receptive fields which covered the most frequently stimulated digital tip surfaces were less than half as large as were those representing the corresponding surfaces of control digits. In a second series of experiments, Long-Evans rats were assigned to environments promoting differential tactile experience (standard, enriched, and impoverished) for 80 to 115 days from the time of weaning. A fourth group of young adult rat experienced a severe restriction of forepaw exploratory movement for either 7 or 15 days. Cortical maps derived in the primary somatosensory cortex showed that environmental enrichment induced a substantial enlargement of the cutaneous forepaw representation, and improved its spatial resolution (smaller glabrous receptive fields). In contrast, tactile impoverishment resulted in a degradation of the forepaw representation that was characterized by larger cutaneous receptive fields and the emergence of non-cutaneous responses. Cortical maps derived in the hemispheres contralateral to the immobilized forelimb exhibited a severe decrease of about 50% in the overall areal extent of the cutaneous representation of the forepaw, which resulted from the invasion of topographically organized cortical zones of non-cutaneous responses, and numerous discontinuities in the representation of contiguous skin territories. The size and the spatial arrangement of the cutaneous receptive fields were not significantly modified by the immobilization of the contralateral forelimb. Similar results were obtained regardless of whether the forelimb restriction lasted 7 or 15 days. These two studies corroborate the view that representational constructs are permanently reshaped by novel experiences through dynamic competitive processes. These studies also support the notion that subject-environment interactions play a crucial role in the maintenance of basic organizational features of somatosensory representations.

Visual experience during a sensitive period plays a critical role in vestibular compensation: neuronal substrates within Deiters' nucleus in the alert cat.

In a previous study [31], we showed that Deiters' neurons ipsilateral to a vestibular neurectomy temporarily exhibit increased sensitivity to visual cues about fast movement. It was proposed that this change in the deafferented vestibular neuron response observed only during the first 3 weeks post-lesion plays an important role in the vestibular compensation process. The present study was aimed at analyzing the potential influence over the first 2 weeks post-lesion of visual motion cue deprivation (cats housed in stroboscopic light) and passive visual experience (visual information not correlated to head or body movement) on the visually induced activity of Deiters' cells. The extra-cellular response of single units was recorded during sinusoidal translation of a whole field optokinetic stimulus in six alert cats. Following the deprivation of visual motion cues, vestibular unit responses were found to be tuned to low frequencies of visual stimulation, as in intact cats, and to display a phase lag re. velocity during rapid visual stimulation. Passive visual stimulation was also found to impede the increase in neuronal sensitivity to visual input, although the cats had benefited from normal vision from the 15th day post-lesion. These results are discussed in relation to the functional implication of interactive visual experience within the early stages (sensitive period) of the vestibular compensation process.

Alterations of the cortical representation of the rat ventrum induced by nursing behavior.

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.

Visual sensory substitution in vestibular compensation: neuronal substrates in the alert cat.

The purpose of this study was to investigate adaptive changes in the activity of vestibular nuclei neurons unilaterally deprived of their primary afferent inputs when influenced by visual motion cues. These neuronal changes might account for the established role that vision plays in the compensation for posturo-kinetic deficits after the loss of vestibular inputs. Neuronal recordings were made in alert, non-paralysed cats that had undergone unilateral vestibular nerve sections. The unit responses collected in both Deiters' nuclei were compared to those previously recorded in intact cats. We analysed the extracellular activity of Deiters' nucleus neurons, as well as the optokinetic reflex (OKR) evoked during sinusoidal translation of a whole-field optokinetic stimulus in the vertical plane. In intact cats, we found the unit firing rate closely correlated with the visual surround translation velocity, and the relationship between the discharge rate and the motion frequency was tuned around an optimal frequency. The maximum firing rate modulation was generally below the 0.25 Hz stimulus frequency; unit responses were weak or even absent above 0.25 Hz. From the 4th day to the end of the 3rd week after ipsilateral deafferentation, a majority of cells was found to display maximum discharge modulation during vertical visual stimulation at 0.50 Hz, and even at 0.75 Hz, indicating that the frequency bandwidth of the visually induced responses of deafferented vestibular nuclei neurons had been extended. Consequently, the frequency-dependent attenuation in the sensitivity of vestibular neurons to visual inputs was much less pronounced. After the first 3 weeks post-lesion, the unit response characteristics were very similar to those observed prior to the deafferentation. On the nucleus contralateral to the neurectomy, the maximum modulation of most cells was tuned to the low frequencies of optokinetic stimulation, as also seen prior to the lesion. We found, however, a subgroup of cells displaying well-developed responses above 0.50 Hz. Under all experimental conditions, the neuronal response phase still remained closely correlated with the motion velocity of the vertical sinusoidal visual pattern. We hypothesize that Deiters' neurons deprived of their primary afferents may transiently acquire the ability to code fast head movements on the basis of visual messages, thus compensating, at least partially, for the loss of dynamic vestibular inputs during the early stages of the recovery process.(ABSTRACT TRUNCATED AT 400 WORDS)