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Long-term modification of cortical synapses improves sensory perception.

ABSTRACT: Synapses and receptive fields of the cerebral cortex are plastic. However, changes to specific inputs must be coordinated within neural networks to ensure that excitability and feature selectivity are appropriately configured for perception of the sensory environment. We induced long-lasting enhancements and decrements to excitatory synaptic strength in rat primary auditory cortex by pairing acoustic stimuli with activation of the nucleus basalis neuromodulatory system. Here we report that these synaptic modifications were approximately balanced across individual receptive fields, conserving mean excitation while reducing overall response variability. Decreased response variability should increase detection and recognition of near-threshold or previously imperceptible stimuli. We confirmed both of these hypotheses in behaving animals. Thus, modification of cortical inputs leads to wide-scale synaptic changes, which are related to improved sensory perception and enhanced behavioral performance.

SUBMITTER: Froemke RC

PROVIDER: S-EPMC3711827 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Long-term modification of cortical synapses improves sensory perception.

Froemke Robert C RC Carcea Ioana I Barker Alison J AJ Yuan Kexin K Seybold Bryan A BA Martins Ana Raquel O AR Zaika Natalya N Bernstein Hannah H Wachs Megan M Levis Philip A PA Polley Daniel B DB Merzenich Michael M MM Schreiner Christoph E CE

Nature neuroscience 20121125 1

Synapses and receptive fields of the cerebral cortex are plastic. However, changes to specific inputs must be coordinated within neural networks to ensure that excitability and feature selectivity are appropriately configured for perception of the sensory environment. We induced long-lasting enhancements and decrements to excitatory synaptic strength in rat primary auditory cortex by pairing acoustic stimuli with activation of the nucleus basalis neuromodulatory system. Here we report that these ...[more]

PMID: 23178974

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Project description:Our ability to integrate multiple sensory-based representations of our surrounding supplies us with a more holistic view of our world. There are many complex algorithms our nervous system uses to construct a coherent perception. An indicator to solve this 'binding problem' are the temporal characteristics with the specificity that environmental information has different propagation speeds (e.g., sound and electromagnetic waves) and sensory processing time and thus the temporal relationship of a stimulus pair derived from the same event must be flexibly adjusted by our brain. This tolerance can be conceptualized in the form of the cross-modal temporal binding window (TBW). Several studies showed the plasticity of the TBW and its importance concerning audio-visual illusions, synesthesia, as well as psychiatric disturbances. Using three audio-visual paradigms, we investigated the importance of length (short vs. long) as well as modality (uni- vs. multimodal) of a perceptual training aiming at reducing the TBW in a healthy population. We also investigated the influence of the TBW on speech intelligibility, where participants had to integrate auditory and visual speech information from a videotaped speaker. We showed that simple sensory trainings can change the TBW and are capable of optimizing speech perception at a very naturalistic level. While the training-length had no different effect on the malleability of the TBW, the multisensory trainings induced a significantly stronger narrowing of the TBW than their unisensory counterparts. Furthermore, a narrowing of the TBW was associated with a better performance in speech perception, meaning that participants showed a greater capacity for integrating informations from different sensory modalities in situations with one modality impaired. All effects persisted at least seven days. Our findings show the significance of multisensory temporal processing regarding ecologically valid measures and have important clinical implications for interventions that may be used to alleviate debilitating conditions (e.g., autism, schizophrenia), in which multisensory temporal function is shown to be impaired.

Project description:Highly correlated firing of primary afferent inputs and lamina I projection neurons evokes synaptic long-term potentiation (LTP), a mechanism by which ascending nociceptive transmission can be amplified at the level of the spinal dorsal horn. However, the degree to which neuromodulatory signaling shapes the temporal window governing spike-timing-dependent plasticity (STDP) at sensory synapses onto projection neurons remains unclear. The present study demonstrates that activation of spinal D1/D5 dopamine receptors (D1/D5Rs) creates a highly permissive environment for the production of LTP in male and female adult mouse spinoparabrachial neurons by promoting non-Hebbian plasticity. Bath application of the mixed D1/D5R agonist SKF82958 unmasked LTP at STDP pairing intervals that normally fail to alter synaptic efficacy. Furthermore, during D1/D5R signaling, action potential discharge in projection neurons became dispensable for LTP generation, and primary afferent stimulation alone was sufficient to induce strengthening of sensory synapses. This non-Hebbian LTP was blocked by the D1/D5R antagonist SCH 39166 or genetic deletion of D5R, and required activation of mGluR5 and intracellular Ca2+ release but was independent of NMDAR activation. D1/D5R-enabled non-Hebbian plasticity was observed across multiple neuronal subpopulations in the superficial dorsal horn but was more prevalent in spinoparabrachial neurons than interneurons. Interestingly, the ability of neonatal tissue damage to promote non-Hebbian LTP in adult projection neurons was not observed in D5R knock-out mice. Collectively, these findings suggest that joint spinal D1/D5R and mGluR5 activation can allow unfettered potentiation of sensory synapses onto the output neurons responsible for conveying pain and itch information to the brain.SIGNIFICANCE STATEMENT Synaptic LTP in spinal projection neurons has been implicated in the generation of chronic pain. Under normal conditions, plasticity at sensory synapses onto adult mouse spinoparabrachial neurons follows strict Hebbian learning rules, requiring coincident presynaptic and postsynaptic firing. Here, we demonstrate that the activation of spinal D1/D5Rs promotes a switch from Hebbian to non-Hebbian LTP so that primary afferent stimulation alone is sufficient to evoke LTP in the absence of action potential discharge in projection neurons, which required joint activation of mGluR5 and intracellular Ca2+ release but not NMDARs. These results suggest that D1/D5Rs cooperate with mGluR5 receptors in the spinal dorsal horn to powerfully influence the amplification of ascending nociceptive transmission to the brain.

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Long-term modification of cortical synapses improves sensory perception.

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Long-term modification of cortical synapses improves sensory perception.

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