Effects of passive tactile co-activation on median ulnar nerve representation in human SI.

In animals simple passive co-activation causes a fusion and expansion of the involved cortical representations. We used passive tactile finger co-activation for 40 min to investigate cortical representational changes in the human somatosensory cortex. Magnetic source imaging revealed that the euclidean distance between median and ulnar nerve somatosensory evoked fields (SEF) was significantly reduced after application of 600 synchronous airpuff stimuli to the fingertips of four fingers. In the control experiment without co-activation no significant change in distance was observed. Perception threshold and spatial two-point discrimination were not affected by the synchronous stimulation. This is in contrast to blind three-finger Braille readers who frequently mislocalize stimuli applied to the reading fingers. This points to a lack of behavioural relevance or the short duration of co-activation.

Tactile coactivation-induced changes in spatial discrimination performance.

We studied coactivation-based cortical plasticity at a psychophysical level in humans. For induction of plasticity, we used a protocol of simultaneous pairing of tactile stimulation to follow as closely as possible the idea of Hebbian learning. We reported previously that a few hours of tactile coactivation resulted in selective and reversible reorganization of receptive fields and cortical maps of the hindpaw representation of the somatosensory cortex of adult rats (Godde et al., 1996). In the present study, simultaneous spatial two-point discrimination was tested on the tip of the right index finger in human subjects as a marker of plastic changes. After 2 hr of coactivation we found a significant improvement in discrimination performance that was reversible within 8 hr. Reduction of the duration of the coactivation protocol revealed that 30 min was not sufficient to drive plastic changes. Repeated application of coactivation over 3 consecutive days resulted in a delayed recovery indicating stabilization of the improvement over time. Perceptual changes were highly selective because no transfer of improved performance to fingers that were not stimulated was found. The results demonstrate the potential role of sensory input statistics (i.e., their probability of occurrence and spatiotemporal relationships) in the induction of cortical plasticity without involving cognitive factors such as attention or reinforcement.

Learning cortical topography from spatiotemporal stimuli.

Stimulus representation is a functional interpretation of early sensory cortices. Early sensory cortices are subject to stimulus-induced modifications. Common models for stimulus-induced learning within topographic representations are based on the stimuli's spatial structure and probability distribution. Furthermore, we argue that average temporal stimulus distances reflect the stimuli's relatedness. As topographic representations reflect the stimuli's relatedness, the temporal structure of incoming stimuli is important for the learning in cortical maps. Motivated by recent neurobiological findings, we present an approach of cortical self-organization that additionally takes temporal stimulus aspects into account. The proposed model transforms average interstimulus intervals into representational distances. Thereby, neural topography is related to stimulus dynamics. This offers a new time-based interpretation of cortical maps. Our approach is based on a wave-like spread of cortical activity. Interactions between dynamics and feedforward activations lead to shifts of neural activity. The psychophysical saltation phenomenon may represent an analogue to the shifts proposed here. With regard to cortical plasticity, we offer an explanation for neurobiological findings that other models cannot explain. Moreover, we predict cortical reorganizations under new experimental, spatiotemporal conditions. With regard to psychophysics, we relate the saltation phenomenon to dynamics and interaction in early sensory cortices and predict further effects in the perception of spatiotemporal stimuli.

Proprioception acts as the main source of input in human S-I activation experiments: a functional MRI study.

During tactile exploration cells in human somatosensory cortex S-I receive input from skin receptors and from proprioceptive feedback. To study the extent to which these sources contribute to cell activation we used functional magnetic resonance imaging (fMRI) in order to visualize the spatial extent and amplitude of activation in S-I during active finger movement and passive stimulation of finger tips. In all subjects (n = 6) we measured activation elicited by unilateral single finger tapping (active task) and mechanical stimulation of the palm of the index finger (passive task). In the finger tapping condition all subjects showed a strict contralateral activation of somatosensory cortex S-I and motor cortex M-I. In the passive stimulation experiment we found activation of the contralateral somatosensory cortex S-I only. Although subjects were trained to perform the finger movement with the same frequency and pressure in comparison to the passive stimulation, the activation within S-I induced by finger movements was always significantly larger than that induced by passive stimulation. This result implies that activation of somatosensory cortex originates to a large extent from proprioception while tactile input plays a minor role in S-I excitation.

Learning transfer and neuronal plasticity in humans trained in tactile discrimination.

Adult humans were unilaterally trained in a tactile discrimination task of sequentially applied multi-finger stimuli. Magnetic source imaging (MSI) was performed before and after the training to evaluate use-dependent neuronal plasticity. All subjects showed fast improvements in performance and complete transfer of the learned task. MSI recordings revealed an unilateral decrease in current dipole strength in the somatosensory system contralateral to the trained hand. Attenuation of sensory evoked fields and a complete learning transfer indicate learning in associative and secondary cortices rather than perceptual plasticity operating on neuronal populations involved in early sensory processing. This findings are discussed with respect to an equivalent animal model and to learning specificity and generalization.

Low-frequency oscillations of visual, auditory and somatosensory cortical neurons evoked by sensory stimulation.

Low-frequency oscillations-LFOs-below 20 Hz in the activity of cortical neurons are a commonly observed property across all sensory modalities. However, the functional significance and potential role of these intrinsic oscillations are not well understood. Here, we attempt to provide a general framework for the interpretation of this phenomenon by considering its properties across several sensory modalities. In the first part, we provide a survey and a general description of low-frequency oscillations (LFOs) at a cellular level observed following adequate [Basar, and Schürmann, 1994]. Sensory stimulation of neurons recorded in three sensory modalities of neocortices in higher mammals. The second part will address some functional aspects of low-frequency oscillations (LFOs) such as stimulus selectivity and so-called 'interference' phenomena, specifically with findings related to 'resetting' and 'gating' of sensory processing streams. Finally, a hypotheses is outlined in which the low-frequency oscillations are regarded as an organizational principle by which continuity of sensory and motor states over time could be accomplished.

Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing.

We studied phenomena, constraints, rules, and implications of cortical plastic reorganization produced by input coactivation patterns in primary somatosensory cortex of adult rats. Intracortical microstimulation (ICMS) and an associative pairing of tactile stimulation (PPTS) induced plastic changes within minutes to hours that were fully reversible. Reorganization of receptive fields and topographic maps was studied with electrophysiologic recordings, mapping techniques, and optical imaging of intrinsic signals. Utilizing the specific advantages of local application of ICMS, we investigated lamina-specific properties of cortical representational plasticity, revealing a prominent role of the input layer IV during plastic reorganization. To study subcortical plasticity, we compared ICMS and intrathalamic microstimulation (ITMS), revealing robust thalamic reorganizations that were, however, much smaller than cortical changes. Using PPTS, we found significant reorganizational processes at the cortical level, including receptive fields, overlap, and cortical representational maps. The protocol was similarly effective at the perceptual level by enhancing the spatial discrimination performance in humans, suggesting that these particular fast plastic processes have perceptual consequences. The implications were discussed with respect to parallel changes of information processing strategies. We addressed the question of the possible role of RF size and size of cortical area, inhibitory mechanisms, and Hebbian and non-Hebbian learning rules. The short time scale of the effects and the aspect of reversibility support the hypothesis of fast modulations of synaptic efficiency without necessarily involving anatomic changes. Such systems of predominantly dynamically maintained cortical and adaptive processing networks may represent the neural basis for life-long adaptational sensory and perceptual capacities and for compensational reorganizations following injuries.

Associative pairing of tactile stimulation induces somatosensory cortical reorganization in rats and humans.

We used a protocol of associative (Hebbian) pairing of tactile stimulation (APTS) to evoke cortical plastic changes. Reversible reorganization of the adult rat paw representations in somatosensory cortex (SI) induced by a few hours of APTS included selective enlargement of the areas of cortical neurones representing the stimulated skin fields and of the corresponding receptive fields (RFs). Late, presumably NMDA receptor-mediated response components were enhanced, indicating an involvement of glutamatergic synapses. A control protocol of identical stimulus pattern applied to only a single skin site revealed no changes of RFs, indicating that co-activation is crucial for induction. Using an analogous APTS protocol in humans revealed an increase of spatial discrimination performance indicating that fast plastic processes based on co-activation patterns act on a cortical and perceptual level.

A columnar model of somatosensory reorganizational plasticity based on Hebbian and non-Hebbian learning rules.

Topographical and functional aspects of neuronal plasticity were studied in the primary somatosensory cortex of adult rats in acute electrophysiological experiments. Under these experimental conditions, we observed short-term reversible reorganization induced by intracortical microstimulation or by an associative pairing of peripheral tactile stimulation. Both types of stimulation generate large-scale and reversible changes of the representational topography and of single cell functional properties. We present a model to simulate the spatial and functional reorganizational aspects of this type of short-term and reversible plasticity. The columnar structure of the network architecture is described and discussed from a biological point of view. The simulated architecture contains three main levels of information processing. The first one is a sensor array corresponding to the sensory surface of the hind paw. The second level, a pre-cortical relay cell array, represents the thalamo-cortical projection with different levels of excitatory and inhibitory relay cells and inhibitory nuclei. The array of cortical columns, the third level, represents stellate, double bouquet, basket and pyramidal cell interactions. The dynamics of the network are ruled by two integro-differential equations of the lateral-inhibition type. In order to implement neuronal plasticity, synaptic weight parameters in those equations are variables. The learning rules are motivated by the original concept of Hebb, but include a combination of both Hebbian and non-Hebbian rules, which modifies different intra- and inter-columnar interactions. We discuss the implications of neuronal plasticity from a behavioral point of view in terms of information processing and computational resources.

Effects of ageing on topographic organization of somatosensory cortex.

Deficits in limb coordination and decreased motor activity have been described in old rats older than 24 months, an approved animal model in ageing research. We investigated the implications of age-related decline of sensorimotor performance by studying the functional cortical organization of aged rats. The cutaneous receptive fields of the hindpaw representations in somatosensory cortex and the cortical areas excited by tactile point-stimulation were enlarged and highly overlapping in old rats when compared with young rats. This gives rise to a complete loss of topographic detail. These functional changes were correlated with the rat's individual walking patterns, indicating that age-related deficits in sensorimotor performance are paralleled by degradation of the functional representations in the ageing nervous system.

Reversible relocation of representational boundaries of adult rats by intracortical microstimulation.

Cortical reorganization of somatosensory maps of adult rats is not restricted to central, already cutaneous zones. A few hours of intracortical microstimulation (ICMS) at the boundaries of the hindpaw representation generated plastic reorganization beyond these functionally defined representational borders by inducing new skin field representations in previously non-somatic cortical regions, from where low-threshold movements could be elicited. In this way, individually defined borders could be reversibly relocated over distances up to 800 microns, containing selectively skin field representations of the ICMS site. Response amplitude and latency characteristics of these newly induced cutaneous recordings sites resembled those recorded under control in the central representational zones. The results suggest that ICMS-induced plasticity acts across areal and modality borders by fast modulation of synapses in overlapping cortical and subcortical networks.

Dynamic properties of cortical evoked (10 Hz) oscillations: theory and experiment.

Experiments probed the dynamic properties of stimulus-evoked (approximately 10 Hz) oscillations in somatosensory cortex of anesthetized rats. Experimental paradigms and statistical time series analysis were based on theoretical ideas from a dynamic approach to temporal patterns of neuronal activity. From the results of a double-stimulus paradigm we conclude that the neuronal response contains two components with different dynamics and different coupling to the stimulus. Based on this result a quantitative dynamic model is derived, making use of normal form theory for bifurcating vector fields. The variables used are abstract, but measurable, dynamic components. The model parameters capture the dynamic properties of neuronal response and are related to experimental results. A structural interpretation of the model can be given in terms of the collective dynamics of neuronal groups, their mutual interaction, and their coupling to peripheral stimuli. The model predicts the stimulus-dependent lifetime of the oscillations as observed in experiment. We show that this prediction relies on the basic concept of dynamic bistability and does not depend on the modeling details.

Evoked oscillatory cortical responses are dynamically coupled to peripheral stimuli.

We report that the response of neurons in rat somatosensory cortex to tactile stimulation consists of two components, a short-latency response and an oscillatory response, observable as up to 8 peaks in the post-stimulus-time-histogram with interpeak intervals in the order of 100 ms (10 Hz). While the first component is always stimulus locked, the second component is strictly stimulus-locked only when elicited from the resting state: once started, the oscillations are only weakly affected by further stimulation. This implies generally that the question of stimulus locking of oscillatory response components is not a yes/no question. Instead, the concept of dynamic coupling is shown to adequately capture the different limit cases. We present a simple dynamic model that exemplifies this point.