Abstract
Can the adult brain assimilate a novel, topographically organized, sensory modality into its perceptual repertoire? To test this, we implemented a microstimulation-based neuroprosthesis that rats used to discriminate among infrared (IR) light sources. This system continuously relayed information from four IR sensors that were distributed to provide a panoramic view of IR sources, into primary somatosensory cortex (S1). Rats learned to discriminate the location of IR sources in <4 d. Animals in which IR information was delivered in spatial register with whisker topography learned the task more quickly. Further, in animals that had learned to use the prosthesis, altering the topographic mapping from IR sensor to stimulating electrode had immediate deleterious effects on discrimination performance. Multielectrode recordings revealed that S1 neurons had multimodal (tactile/IR) receptive fields, with clear preferences for those stimuli most likely to be delivered during the task. Neuronal populations predicted, with high accuracy, which stimulation pattern was present in small (75 ms) time windows. Surprisingly, when identical microstimulation patterns were delivered during an unrelated task, cortical activity in S1 was strongly suppressed. Overall, these results show that the adult mammalian neocortex can readily absorb completely new information sources into its representational repertoire, and use this information in the production of adaptive behaviors.
SIGNIFICANCE STATEMENT Understanding the potential for plasticity in the adult brain is a key goal for basic neuroscience and modern rehabilitative medicine. Our study examines one dimension of this challenge: how malleable is sensory processing in adult mammals? We implemented a panoramic infrared (IR) sensory prosthetic system in rats; it consisted of four IR sensors equally spaced around the circumference of the head of the rat. Each sensor was coupled to a microstimulating electrode placed in the somatosensory cortex of the rat. Within days, rats learned to use the prosthesis to track down items associated with IR light in their environment. This is quite promising clinically, as the largest demand for sensory prosthetic devices is in adults whose brains are already fully developed.
