Use of a cortical neuroprosthesis to detect invisible light generates infrared light representations in two somatosensory thalamic nuclei

Previous research has demonstrated that rats can learn to utilize a neuroprosthetic device to track infrared (IR) light sources outside their normal visual range. This device delivers IR information directly to the somatosensory cortex (S1) via intracortical microstimulation (ICMS). While S1 neurons have been shown to develop IR receptive fields, the role of the thalamus in processing this novel sensory input remains unclear. This study aimed to investigate the involvement of the thalamus in integrating IR sensory information and the emergence of IR representations within thalamocortical circuits. Adult rats were implanted with a cortical neuroprosthesis delivering IR-driven ICMS to bilateral S1. Neural activity was simultaneously recorded from left and right hemispheres of S1 and right thalamic (ventral posterior medial [VPM], posterior medial [POM]) nuclei during an IR-guided behavioral task. IR receptive fields were characterized using information-theoretic analysis. Neural ensemble coding was evaluated using machine learning classification. Widespread activation in response to ICMS was observed across all recorded regions. The percentage of neurons with significant mutual information between firing activity and IR stimulus features ranged from 56.2% to 74.2%. VPM ensembles demonstrated superior decoding performance for IR information compared to S1 ensembles in a support vector classification model, requiring fewer neurons to achieve similar accuracy (43.1 vs. 55.0 neurons, Tukey’s HSD, P ​<0.05). Importantly, animals retained the ability to process tactile information and recorded neurons were found to respond to whisker stimulation. These findings demonstrate the rapid adaptation of thalamocortical circuits to represent a novel sensory modality and suggest a major role of the thalamus in processing the prosthetic sensation. Furthermore, these results suggest that ICMS-based neuroprostheses recruit neurons from the entire sensory pathway without compromising the endogenous sensory function.