Abstract

Adult learning-induced sensory cortex plasticity results in enhanced action potential rates in neurons that have the most relevant information for the task, or those that respond strongly to one sensory stimulus but weakly to its comparison stimulus. Current theories suggest this plasticity is caused when target stimulus evoked activity is enhanced by reward signals from neuromodulatory nuclei. Prior work has found evidence suggestive of nonselective enhancement of neural responses, and suppression of responses to task distractors, but the differences in these effects between detection and discrimination have not been directly tested. Using cortical implants, we defined physiological responses in macaque somatosensory cortex during serial, matched, detection and discrimination tasks. Nonselective increases in neural responsiveness were observed during detection learning. Suppression of responses to task distractors was observed during discrimination learning, and this suppression was specific to cortical locations that sampled responses to the task distractor before learning. Changes in receptive field size were measured as the area of skin that had a significant response to a constant magnitude stimulus, and these areal changes paralleled changes in responsiveness. From before detection learning until after discrimination learning, the enduring changes were selective suppression of cortical locations responsive to task distractors, and nonselective enhancement of responsiveness at cortical locations selective for target and control skin sites. A comparison of observations in prior studies with the observed plasticity effects suggests that the non-selective response enhancement and selective suppression suffice to explain known plasticity phenomena in simple spatial tasks. This work suggests that differential responsiveness to task targets and distractors in primary sensory cortex for a simple spatial detection and discrimination task arise from nonselective increases in response over a broad cortical locus that includes the representation of the task target, and selective suppression of responses to the task distractor within this locus.

Highlights

  • The adult brain learns to discriminate somatosensory, auditory, and visual forms through experience

  • The reinforcement process could be unimodal and selectively enhance the most informative neurons. This strategy, requires a reinforcement process that can differentiate between high levels of neural activity, or the neural response to the target, and lower levels of neural activity that are more informative about reinforcement, or neural responses that differentiate the target and distractor

  • An array of 64 microelectrodes was implanted into the primary somatosensory cortex of two adult Rhesus monkeys, and responses were allowed to stabilize for more than six weeks

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Summary

Introduction

The adult brain learns to discriminate somatosensory, auditory, and visual forms through experience. Neurons that respond to stimuli associated with reward develop stronger responses throughout practice, whereas neurons associated with omission of reward exhibit weaker responses after experience This learning rule implies that neurons carrying the most reward–relevant information, or those that respond strongly to the target and weakly to the distractor, will have their responsiveness enhanced [10,12,14,15,16,17,18], and that neurons are impacted by associational learning [11]. The neuromodulators, which are released in sensory cortex after stimuli associated with reward, act to potentiate the responses to task targets [23,24,25,26,27,28,29] This mechanism is plausible and backed by data, it requires additional mechanisms to potentiate informative responses, and not just target stimulus responses

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