Eric E. Thomson

Perceiving Invisible Light through a Somatosensory Cortical Prosthesis

Sensory neuroprostheses show great potential for alleviating major sensory deficits. It is not known, however, whether such devices can augment the subject’s normal perceptual range. Here we show that adult rats can learn to perceive otherwise invisible infrared (IR) light through a neuroprosthesis that couples the output of a head-mounted IR sensor to their somatosensory cortex (S1) via intracortical microstimulation (ICMS). Rats readily learn to use this new information source, and generate active exploratory strategies to discriminate among IR sources in their environment. S1 neurons in these IR-perceiving rats respond to both whisker deflection and ICMS, suggesting that the IR representation does not displace the original tactile representation. Hence, sensory cortical prostheses, in addition to restoring normal neurological functions, may serve to expand natural perceptual capabilities in mammals.

Quantifying Stimulus Discriminability: A Comparison of Information Theory and Ideal Observer Analysis

Performance in sensory discrimination tasks is commonly quantified using either information theory or ideal observer analysis. These two quantitative frameworks are often assumed to be equivalent. For example, higher mutual information is said to correspond to improved performance of an ideal observer in a stimulus estimation task. To the contrary, drawing on and extending previous results, we show that five information-theoretic quantities (entropy, response-conditional entropy, specific information, equivocation, and mutual information) violate this assumption. More positively, we show how these information measures can be used to calculate upper and lower bounds on ideal observer performance, and vice versa. The results show that the mathematical resources of ideal observer analysis are preferable to information theory for evaluating performance in a stimulus discrimination task. We also discuss the applicability of information theory to questions that ideal observer analysis cannot address.

Changes in S1 Neural Responses During Tactile Discrimination Learning

In freely moving rats that are actively performing a discrimination task, single-unit responses in primary somatosensory cortex (S1) are strikingly different from responses to comparable tactile stimuli in immobile rats. For example, in the active discrimination context prestimulus response modulations are common, responses are longer in duration and more likely to be inhibited. To determine whether these differences emerge as rats learned a whisker-dependent discrimination task, we recorded single-unit S1 activity while rats learned to discriminate aperture-widths using their whiskers. Even before discrimination training began, S1 responses in freely moving rats showed many of the signatures of active responses, such as increased duration of response and prestimulus response modulations. As rats subsequently learned the discrimination task, single unit responses changed: more cortical units responded to the stimuli, neuronal sensory responses grew in duration, and individual neurons better predicted aperture-width. In summary, the operant behavioral context changes S1 tactile responses even in the absence of tactile discrimination, whereas subsequent width discrimination learning refines the S1 representation of aperture-width.

Encoding and Decoding Touch Location in the Leech CNS

Spike times encode stimulus values in many sensory systems, but it is generally unknown whether such temporal variations are decoded (i.e., whether they influence downstream networks that control behavior). In the present study, we directly address this decoding problem by quantifying both sensory encoding and decoding in the leech. By mechanically stimulating the leech body wall while recording from mechanoreceptors, we show that pairs of leech sensory neurons with overlapping receptive fields encode touch location by their relative latencies, number of spikes, and instantaneous firing rates, with relative latency being the most accurate indicator of touch location. We then show that the relative latency and count are decoded by manipulating these variables in sensory neuron pairs while simultaneously monitoring the resulting behavior. Although both variables are important determinants of leech behavior, the decoding mechanisms are more sensitive to changes in relative spike count than changes in relative latency.

Basal forebrain dynamics during a tactile discrimination task

The nucleus basalis (NB) is a cholinergic neuromodulatory structure that projects liberally to the entire cortical mantle and regulates information processing in all cortical layers. Here, we recorded activity from populations of single units in the NB as rats performed a whisker-dependent tactile discrimination task. Over 80% of neurons responded with significant modulation in at least one phase of the task. Such activity started before stimulus onset and continued for seconds after reward delivery. Firing rates monotonically increased with reward magnitude during the task, suggesting that NB neurons are not indicating the absolute deviation from expected reward amounts. Individual neurons also encoded significant amounts of information about stimulus identity. Such robust coding was not present when the same stimuli were delivered to lightly anesthetized animals, suggesting that the NB neurons contain a sensorimotor, rather than purely sensory or motor, representation of the environment. Overall, these results support the hypothesis that neurons in the NB provide a value-laden representation of the sensorimotor state of the animal as it engages in significant behavioral tasks.

Embedding a Panoramic Representation of Infrared Light in the Adult Rat Somatosensory Cortex through a Sensory Neuroprosthesis

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.

Neural Representations Observed

The historical debate on representation in cognitive science and neuroscience construes representations as theoretical posits and discusses the degree to which we have reason to posit them. We reject the premise of that debate. We argue that experimental neuroscientists routinely observe and manipulate neural representations in their laboratory. Therefore, neural representations are as real as neurons, action potentials, or any other well-established entities in our ontology.

Cortical Neuroprosthesis Merges Visible And Invisible Light Without Impairing Native Sensory Function

Abstract Adult rats equipped with a sensory prosthesis, which transduced infrared (IR) signals into electrical signals delivered to somatosensory cortex (S1), took approximately 4 d to learn a four-choice IR discrimination task. Here, we show that when such IR signals are projected to the primary visual cortex (V1), rats that are pretrained in a visual-discrimination task typically learn the same IR discrimination task on their first day of training. However, without prior training on a visual discrimination task, the learning rates for S1- and V1-implanted animals converged, suggesting there is no intrinsic difference in learning rate between the two areas. We also discovered that animals were able to integrate IR information into the ongoing visual processing stream in V1, performing a visual-IR integration task in which they had to combine IR and visual information. Furthermore, when the IR prosthesis was implanted in S1, rats showed no impairment in their ability to use their whiskers to perform a tactile discrimination task. Instead, in some rats, this ability was actually enhanced. Cumulatively, these findings suggest that cortical sensory neuroprostheses can rapidly augment the representational scope of primary sensory areas, integrating novel sources of information into ongoing processing while incurring minimal loss of native function.

Twenty-Five Years of Multielectrode Recordings in the Somatosensory System: It is All about Dynamics

Chronic multielectrode recording methods introduced 25 years ago have opened up the opportunity to simultaneously sample the activity of neurons at multiple levels of the somatosensory system while rats engage in active tactile behaviors. This chapter focuses on results gleaned from recordings in the rat whisker system. The earliest multielectrode investigations revealed that the peak of neural activity evoked by single-whisker stimuli drifts widely over the cortical and thalamic somatotopic whisker maps. This property could provide a mechanism for recognizing spatiotemporal patterns of whisker stimulation. These studies also showed that information about tactile stimulus identity is carried by the relative latencies of evoked spikes in different simultaneously recorded neurons. Subsequent experiments also revealed highly synchronized firing in neurons from brainstem to cortex, and immediate receptive field reorganization in thalamus induced by partial deafferentation or reversible inactivation of primary somatosensory cortex (S1). Even the two hemispheres of S1, long viewed as independent modules for processing exclusively contralateral stimuli, were found to interact on millisecond timescales in anesthetized and waking rats. This later finding suggested that the brain combines bilateral whisker afferents to discriminate bilateral whisker stimuli – such as the widths of tunnel openings in the dark – an idea that was confirmed by the development of bilateral tactile discrimination tasks. Multielectrode recordings during tactile discrimination revealed qualitatively distinct response modes in S1 as compared to responses to passive whisker stimulation, including task-related firing rate modulations that begin well before whisker stimulation. These data have pushed our conception of somatosensory representation – even at the earliest thalamic and cortical processing stages – away from the static classical one-barrel/one-whisker picture, toward that of a highly plastic multilevel structure whose functional architecture quickly adjusts to meet the demands of the present situation.