Spike-Timing-Dependent Plasticity in the Intact Brain: Counteracting Spurious Spike Coincidences

A computationally rich algorithm of synaptic plasticity has been proposed based on the experimental observation that the sign and amplitude of the change in synaptic weight is dictated by the temporal order and temporal contiguity between pre- and postsynaptic activities. For more than a decade, this spike-timing-dependent plasticity (STDP) has been studied mainly in brain slices of different brain structures and cultured neurons. Although not yet compelling, evidences for the STDP rule in the intact brain, including primary sensory cortices, have been provided lastly. From insects to mammals, the presentation of precisely timed sensory inputs drives synaptic and functional plasticity in the intact central nervous system, with similar timing requirements than the in vitro defined STDP rule. The convergent evolution of this plasticity rule in species belonging to so distant phylogenic groups points to the efficiency of STDP, as a mechanism for modifying synaptic weights, as the basis of activity-dependent development, learning and memory. In spite of the ubiquity of STDP phenomena, a number of significant variations of the rule are observed in different structures, neuronal types and even synapses on the same neuron, as well as between in vitro and in vivo conditions. In addition, the state of the neuronal network, its ongoing activity and the activation of ascending neuromodulatory systems in different behavioral conditions have dramatic consequences on the expression of spike-timing-dependent synaptic plasticity, and should be further explored

A Re-Examination of Hebbian-Covariance Rules and Spike Timing-Dependent Plasticity in Cat Visual Cortex in vivo

Spike timing-dependent plasticity (STDP) is considered as an ubiquitous rule for associative plasticity in cortical networks in vitro. However, limited supporting evidence for its functional role has been provided in vivo. In particular, there are very few studies demonstrating the co-occurrence of synaptic efficiency changes and alteration of sensory responses in adult cortex during Hebbian or STDP protocols. We addressed this issue by reviewing and comparing the functional effects of two types of cellular conditioning in cat visual cortex. The first one, referred to as the “covariance” protocol, obeys a generalized Hebbian framework, by imposing, for different stimuli, supervised positive and negative changes in covariance between postsynaptic and presynaptic activity rates. The second protocol, based on intracellular recordings, replicated in vivo variants of the theta-burst paradigm (TBS), proven successful in inducing long-term potentiation in vitro. Since it was shown to impose a precise correlation delay between the electrically activated thalamic input and the TBS-induced postsynaptic spike, this protocol can be seen as a probe of causal (“pre-before-post”) STDP. By choosing a thalamic region where the visual field representation was in retinotopic overlap with the intracellularly recorded cortical receptive field as the afferent site for supervised electrical stimulation, this protocol allowed to look for possible correlates between STDP and functional reorganization of the conditioned cortical receptive field. The rate-based “covariance protocol” induced significant and large amplitude changes in receptive field properties, in both kitten and adult V1 cortex. The TBS STDP-like protocol produced in the adult significant changes in the synaptic gain of the electrically activated thalamic pathway, but the statistical significance of the functional correlates was detectable mostly at the population level. Comparison of our observations with the literature leads us to re-examine the experimental status of spike timing-dependent potentiation in adult cortex. We propose the existence of a correlation-based threshold in vivo, limiting the expression of STDP-induced changes outside the critical period, and which accounts for the stability of synaptic weights during sensory cortical processing in the absence of attention or reward-gated supervision

Rich spatio-temporal stimulus dynamics unveil sensory specialization in cortical area S2.

International audienceTactile perception in rodents depends on simultaneous, multi-whisker contacts with objects. Although it is known that neurons in secondary somatosensory cortex (wS2) respond to individual deflections of many whiskers, wS2's precise function remains unknown. The convergence of information from multiple whiskers into wS2 neurons suggests that they are good candidates for integrating multi-whisker information. Here, we apply stimulation patterns with rich dynamics simultaneously to 24 macro-vibrissae of rats while recording large populations of single neurons. Varying inter-whisker correlations without changing single whisker statistics, we observe pronounced supra-linear multi-whisker integration. Using novel analysis methods, we show that continuous multi-whisker movements contribute to the firing of wS2 neurons over long temporal windows, facilitating spatio-temporal integration. In contrast, primary cortex (wS1) neurons encode fine features of whisker movements on precise temporal scales. These results provide the first description of wS2's representation during multi-whisker stimulation and outline its specialized role in parallel to wS1 tactile processing

A celebration of Franco-Argentinean neuroscience

Fil: Calvo, Daniel Juan. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Golombek, Diego Andrés. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Nacional de Quilmes; ArgentinaFil: Shulz, Daniel E.. No especifica

Spatiotemporal properties of whisker-evoked tactile responses in the mouse secondary somatosensory cortex

International audienceThe representation of rodents' mystacial vibrissae within the primary somatosensory (S1) cortex has become a major model for studying the cortical processing of tactile sensory information. However, upon vibrissal stimulation, tactile information first reaches S1 but also, almost simultaneously, the secondary somatosensory cortex (S2). To further understand the role of S2 in the processing of whisker inputs, it is essential to characterize the spatio-temporal properties of whisker-evoked response dynamics in this area. Here we describe the topography of the whiskers representation in the mouse S2 with voltage sensitive dye imaging. Analysis of the spatial properties of the early S2 responses induced by stimulating individually 22 to 24 whiskers revealed that they are spatially ordered in a mirror symmetric map with respect to S1 responses. Evoked signals in S2 and S1 are of similar amplitude and closely correlated at the single trial level. They confirm a short delay (~3 ms) between S1 and S2 early activation. In both S1 and S2 caudo-dorsal whiskers induce stronger responses than rostro-ventral ones. Finally, analysis of early C2-evoked responses indicates a faster activation of neighboring whisker representations in S2 relative to S1, probably due to the reduced size of the whisker map in S2

Representation of Tactile Scenes in the Rodent Barrel Cortex

International audienceAfter half a century of research, the sensory features coded by neurons of the rodent barrel cortex remain poorly understood. Still, views of the sensory representation of whisker information are increasingly shifting from a labeled line representation of single-whisker deflections to a selectivity for specific elements of the complex statistics of the multi-whisker deflection patterns that take place during spontaneous rodent behavior - so called natural tactile scenes. Here we review the current knowledge regarding the coding of patterns of whisker stimuli by barrel cortex neurons, from responses to single-whisker deflections to the representation of complex tactile scenes. A number of multi-whisker tunings have already been identified, including center-surround feature extraction, angular tuning during edge-like multi-whisker deflections, and even tuning to specific statistical properties of the tactile scene such as the level of correlation across whiskers. However, a more general model of the representation of multi-whisker information in the barrel cortex is still missing. This is in part because of the lack of a human intuition regarding the perception emerging from a whisker system, but also because in contrast to other primary sensory cortices such as the visual cortex, the spatial feature selectivity of barrel cortex neurons rests on highly nonlinear interactions that remained hidden to classical receptive field approaches

Bilateral Discrimination of Tactile Patterns without Whisking in Freely Running Rats

International audienceA majority of whisker discrimination tasks in rodents are performed on head-fixed animals to facilitate tracking or control of the sensory inputs. However, head fixation critically restrains the behavior and thus the incoming stimuli compared with those occurring in natural conditions. In this study, we investigated whether freely behaving rats can discriminate fine tactile patterns while running, in particular when stimuli are presented simultaneously on both sides of the snout. We developed a two-alternative forced-choice task in an automated modified T-maze. Stimuli were either a surface with no bars (smooth) or with vertical bars spaced irregularly or regularly. While running at full speed, rats encountered simultaneously the two discriminanda placed on the two sides of the central aisle. Rats learned to recognize regular bars versus a smooth surface in 8 weeks. They solved the task while running at an average speed of 1 m/s, so that the contact with the stimulus lasted <1 typical whisking cycle, precluding the use of active whisking. Whisker-tracking analysis revealed an asymmetry in the position of the whiskers: they oriented toward the rewarded stimulus during successful trials as early as 60 ms after the first possible contact. We showed that the whiskers and activity in the primary somatosensory cortex are involved during the discrimination process. Finally, we identified irregular patterns of bars that the rats can discriminate from the regular one. This novel task shows that freely moving rodents can make simultaneous bilateral tactile discrimination without whisking.SIGNIFICANCE STATEMENT The whisker system of rodents is a widely used model to study tactile processing. Rats show remarkable abilities in discriminating surfaces by actively moving their whiskers (whisking) against stimuli, typically sampling them several times. This motor strategy affects considerably the way that tactile information is acquired and thus the way that neuronal networks process the information. However, when rats run at high speed, they protract their whiskers in front of the snout without large movements. Here, we investigated whether rats are able to discriminate regular and irregular patterns of vertical bars while running without whisking. We found that the animals can perform a bilateral simultaneous discrimination without whisking and that this involves both whiskers and barrel cortex activity

Supra-barrel Distribution of Directional Tuning for Global Motion in the Mouse Somatosensory Cortex

Summary: Rodents explore their environment with an array of whiskers, inducing complex patterns of whisker deflections. Cortical neuronal networks can extract global properties of tactile scenes. In the primary somatosensory cortex, the information relative to the global direction of a spatiotemporal sequence of whisker deflections can be extracted at the single neuron level. To further understand how the cortical network integrates multi-whisker inputs, we imaged and recorded the mouse barrel cortex activity evoked by sequences of multi-whisker deflections generating global motions in different directions. A majority of barrel-related cortical columns show a direction preference for global motions with an overall preference for caudo-ventral directions. Responses to global motions being highly sublinear, the identity of the first deflected whiskers is highly salient but does not seem to determine the global direction preference. Our results further demonstrate that the global direction preference is spatially organized throughout the barrel cortex at a supra-columnar scale. : Using voltage-sensitive dye imaging of the mouse barrel cortex, Vilarchao et al. demonstrate the presence of direction selectivity to global motion generated by multi-whisker stimuli. Selectivity to global motion is spatially organized at the supra-columnar scale with an overrepresentation of selectivity to caudo-ventral directions. Keywords: tactile sensory processing, multivibrissal stimulation, primary somatosensory cortex, barrel cortex, voltage-sensitive dye imaging, mouse, extracellular electrophysiological recording