Friederike Spengler

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.

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 rats individual walking patterns, indicating that age-related deficits in sensorimotor performance are paralleled by degradation of the functional representations in the ageing nervous system.

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.

Learning cortical topography from spatiotemporal stimuli

Abstract. 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 stimulis spatial structure and probability distribution. Furthermore, we argue that average temporal stimulus distances reflect the stimulis relatedness. As topographic representations reflect the stimulis 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.

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.

Receptive field scatter, topography and map variability in different layers of the hindpaw representation of rat somatosensory cortex

We recorded neurons extracellularly in layers II/III, IV, and V of the hindpaw representation of primary somatosensory cortex in anesthetized rats and studied laminar features of receptive fields (RFs) and representational maps. On average, RFs were smallest in layer IV and largest in layer V; however, for individual penetrations we found substantial deviations from this rule. Within the hindpaw representation, a distinct rostrocaudal gradient of RF size was present in all layers. While layer V RFs were generally largest independent of this gradient, layer IV RFs recorded caudally representing the proximal portions of the paw were larger than layer II/III RFs recorded rostrally representing the digits. The individual scatter of the locations of RFs across laminar groups was in the range of several millimeters, corresponding to about 25% of the average RF diameter. The cutaneous representations of the hindpaw in extragranular layers were confined to the areal extent defined by responsive sites in layer IV. Comparison between RFs determined quantitatively and by handplotting showed a reliable correspondence. Repeated measurements of RFs revealed spontaneous fluctuations of RF size of no more than 5% of the initial condition over an observation period of several hours. The topography and variability of cortical maps of the hindpaw representation were studied with a quantitative interpolation method taking into account the geometric centers of RFs and the corresponding cortical recording sites. On average, the overall topography in terms of preservation of neighborhood relations was present in all layers, although some individual maps showed severe distortions of topography. Factors contributing to map variability were overall position of the representation on the cortical surface, internal topography and spatial extent. Interindividual variability of map layout was always highest in the digit representations. Local topographic orderliness was lowest in layer V, but comparable in layers II/III and IV. Within layer IV, the lowest orderliness was observed in the digit representations. Our data emphasize a substantial variability of RF size, overlap and position across layers and within layers. At the level of representational maps, we found a similar degree of variability that often co-varied across layers, with little evidence for significant layer specificity. Laminar differences are likely to arise from the specific input-output pattern, layer-specific cell types and the connectivity between different layers. Our findings emphasizing similarities in the variability across layers support the notion of tightly coupled columnar interactions between different layers.

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.

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.

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

Experiments probed the dynamic properties of stimulus-evoked (≈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 stimulusdependent 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.

A Model of Cortical Plasticity: Integration and Segregation based on Temporal Input Patterns

Early cortical areas reveal plastic topographic structures. The formation and alteration of these so-called cortical maps by self-organizing principles is often explained by Kohonen-like algorithms [7]. However, recent experiments concerning learning related reorganization of Area 3b of somatosensory cortex [1, 2] demonstrate task-specific cortical changes which cannot be explained by Kohonen’s model. We therefore propose a model of stimulus induced cortical plasticity that takes the temporal structure of afferent inputs into account, i.e. temporal stimulus distances are transformed into spatial distances of their cortical representations. The simulations agree with the above cited experimental results and predict the alteration of sensory cortices for different sequences of input patterns.