RESUMEN
Complex body movements require complex dynamics and coordination among neurons in motor cortex. Conversely, a long-standing theoretical notion supposes that if many neurons in motor cortex become excessively synchronized, they may lack the necessary complexity for healthy motor coding. However, direct experimental support for this idea is rare and underlying mechanisms are unclear. Here we recorded three-dimensional body movements and spiking activity of many single neurons in motor cortex of rats with enhanced synaptic inhibition and a transgenic rat model of Rett syndrome (RTT). For both cases, we found a collapse of complexity in the motor system. Reduced complexity was apparent in lower-dimensional, stereotyped brain-body interactions, neural synchrony, and simpler behavior. Our results demonstrate how imbalanced inhibition can cause excessive synchrony among movement-related neurons and, consequently, a stereotyped motor code. Excessive inhibition and synchrony may underlie abnormal motor function in RTT.
Asunto(s)
Encéfalo/fisiopatología , Proteína 2 de Unión a Metil-CpG/genética , Proteína 2 de Unión a Metil-CpG/fisiología , Actividad Motora/genética , Actividad Motora/fisiología , Síndrome de Rett/genética , Síndrome de Rett/fisiopatología , Potenciales de Acción/genética , Potenciales de Acción/fisiología , Animales , Modelos Animales de Enfermedad , Fenómenos Electrofisiológicos , Femenino , Técnicas de Silenciamiento del Gen , Humanos , Masculino , Proteína 2 de Unión a Metil-CpG/deficiencia , Modelos Neurológicos , Corteza Motora/fisiopatología , Neuronas Motoras/fisiología , Ratas , Ratas Sprague-Dawley , Ratas Transgénicas , Conducta Estereotipada/fisiologíaRESUMEN
Cortical neurons can be strongly or weakly coupled to the network in which they are embedded, firing in sync with the majority or firing independently. Both these scenarios have potential computational advantages in motor cortex. Commands to the body might be more robustly conveyed by a strongly coupled population, whereas a motor code with greater information capacity could be implemented by neurons that fire more independently. Which of these scenarios prevails? Here we measure neuron-to-body coupling and neuron-to-population coupling for neurons in motor cortex of freely moving rats. We find that neurons with high and low population coupling coexist, and that population coupling was tunable by manipulating inhibitory signaling. Importantly, neurons with different population coupling tend to serve different functional roles. Those with strong population coupling are not involved with body movement. In contrast, neurons with high neuron-to-body coupling are weakly coupled to other neurons in the cortical population.