Spike timing-dependent plasticity (STDP) is a computationally powerful form of plasticity in which synapses are strengthened or weakened according to the temporal order and precise millisecond-scale delay between presynaptic and postsynaptic spiking activity. STDP is readily observed in vitro, but evidence for STDP in vivo is scarce. Here, we studied spike timing-dependent synaptic depression in single putative pyramidal neurons of the rat primary somatosensory cortex (S1) in vivo, using two techniques. First, we recorded extracellularly from layer 2/3 (L2/3) and L5 neurons, and paired spontaneous action potentials (postsynaptic spikes) with subsequent subthreshold deflection of one whisker (to drive presynaptic afferents to the recorded neuron) to produce "post-leading-pre" spike pairings at known delays. Short delay pairings (Ͻ17 ms) resulted in a significant decrease of the extracellular spiking response specific to the paired whisker, consistent with spike timing-dependent synaptic depression. Second, in whole-cell recordings from neurons in L2/3, we paired postsynaptic spikes elicited by direct-current injection with subthreshold whisker deflection to drive presynaptic afferents to the recorded neuron at precise temporal delays. Post-leading-pre pairing (Ͻ33 ms delay) decreased the slope and amplitude of the PSP evoked by the paired whisker, whereas "pre-leading-post" delays failed to produce depression, and sometimes produced potentiation of whiskerevoked PSPs. These results demonstrate that spike timing-dependent synaptic depression occurs in S1 in vivo, and is therefore a plausible plasticity mechanism in the sensory cortex.
As in other sensory modalities, one function of the somatosensory system is to detect coherence and contrast in the environment. To investigate the neural bases of these computations, we applied different spatiotemporal patterns of stimuli to rat whiskers while recording multiple neurons in the barrel cortex. Model-based analysis of the responses revealed different coding schemes according to the level of input correlation. With uncorrelated stimuli on 24 whiskers, we identified two distinct functional categories of neurons, analogous in the temporal domain to simple and complex cells of the primary visual cortex. With correlated stimuli, however, a complementary coding scheme emerged: two distinct cell populations, similar to reinforcing and antagonist neurons described in the higher visual area MT, responded specifically to correlations. We suggest that similar context-dependent coexisting coding strategies may be present in other sensory systems to adapt sensory integration to specific stimulus statistics.
Neuronal activity plays an important role in the development of the visual pathway. The modulation of synaptic transmission by temporal correlation between pre- and postsynaptic activity is one mechanism which could underly visual cortical plasticity. We report here that functional changes in single neurons of area 17, analogous to those known to take place during epigenesis of visual cortex, can be induced experimentally during the time of recording. This was done by a differential pairing procedure, during which iontophoresis was used to artificially increase the visual response for a given stimulus, and to decrease (or block) the response for a second stimulus which differed in ocularity or orientation. Long-term modifications in ocular dominance and orientation selectivity were produced in 33% and 43% of recorded cells respectively. Neuronal selectivity was nearly always displaced towards the stimulus paired with the reinforced visual response. The largest changes were obtained at the peak of the critical period in normally reared and visually deprived kittens, but changes were also observed in adults. Our findings support the role of temporal correlation between pre- and postsynaptic activity in the induction of long-lasting modifications of synaptic transmission during development, and in associative learning.
Rats use their whiskers to extract a wealth of information about their immediate environment, such as the shape, position or texture of an object. The information is conveyed to mechanoreceptors located within the whisker follicle in the form of a sequence of whisker deflections induced by the whisker/object contact interaction. How the whiskers filter and shape the mechanical information and effectively participate in the coding of tactile features remains an open question to date. In the present article, a biomechanical model was developed that provides predictions of the whisker dynamics during active tactile exploration, amenable to quantitative experimental comparison. This model is based on a decomposition of the whisker profile into a slow, quasi-static sequence and rapid resonant small-scale vibrations. It was applied to the typical situation of a rat actively whisking across a solid object. Having derived the quasi-static sequence of whisker deformation, the resonant properties of the whisker were analyzed, taking into account the boundary conditions imposed by the whisker/surface contact. We then focused on two elementary mechanical events that are expected to trigger significant neural responses, namely (1) the whisker/object first contact and (2) the whisker detachment from the object. Both events were found to trigger a deflection wave propagating upward to the mystacial pad at constant velocity of ≈3–5 m/s. This yielded a characteristic mechanical signature at the whisker base, in the form of a large peak of negative curvature occurring ≈4 ms after the event has been triggered. The dependence in amplitude and lag of this mechanical signal with the main contextual parameters (such as radial or angular distance) was investigated. The model was validated experimentally by comparing its predictions to high-speed video recordings of shock-induced whisker deflections performed on anesthetized rats. The consequences of these results on possible tactile encoding schemes are briefly discussed.
Rats discriminate objects by scanning their surface with the facial vibrissae, producing spatiotemporally complex sequences of tactile contacts. The way in which the somatosensory cortex responds to these complex multivibrissal stimuli has not been explored. It is unclear yet whether contextual information from across the entire whisker pad influences cortical responses. Here, we delivered tactile stimuli to the rat vibrissae using a new 24 whisker stimulator. We tested sequences of rostrocaudal whisker deflections that generate multivibrissal motion patterns in different directions across the mystacial pad, allowing to disambiguate local from global sensory integration. Unitary electrophysiological recordings from different layers of the barrel cortex showed that a majority of neurons has direction selectivity for the multivibrissal stimulus. The selectivity resulted from nonlinear integration of responses across the mystacial pad. Our results indicate that the system extracts collective properties of a tactile scene.
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