Neural Coding of Whisker-Mediated Touch in Primary Somatosensory Cortex Is Altered Following Early Blindness

Abstract

Sensory systems do not develop and function independently of one another, yet they are typically studied in isolation. Effects of multisensory interactions on the developing neocortex can be revealed by altering the ratios of incoming sensory inputs associated with different modalities. We investigated neural responses in primary somatosensory cortex (S1) of short-tailed opossums (; either sex) after the elimination of visual input through bilateral enucleation very early in development. To assess the influence of tactile experience after vision loss, we also examined naturally occurring patterns of exploratory behavior. In early blind (EB) animals, overall levels of tactile experience were similar to those of sighted controls (SC); locomotor activity was unimpaired and accompanied by whisking. Using extracellular single-unit recording techniques under anesthesia, we found that EB animals exhibited a reduction in the magnitude of neural responses to whisker stimuli in S1, coupled with spatial sharpening of receptive fields, in comparison to SC animals. These alterations manifested as two different effects on sensory processing in S1 of EB animals: the ability of neurons to detect single whisker stimulation was decreased, whereas their ability to discriminate between stimulation of neighboring whiskers was enhanced. The increased selectivity of S1 neurons in EB animals was reflected in improved population decoding performance for whisker stimulus position, particularly along the rostrocaudal axis of the snout, which aligns with the primary axis of natural whisker motion. These findings suggest that a functionally distinct form of somatosensory plasticity occurs when vision is lost early in development. After sensory loss, compensatory behavior mediated through the spared senses could be generated entirely through the recruitment of brain areas associated with the deprived sense. Alternatively, functional compensation in spared modalities may be achieved through a combination of plasticity in brain areas corresponding to both spared and deprived sensory modalities. Although activation of neurons in cortex associated with a deprived sense has been described frequently, it is unclear whether this is the only substrate available for compensation or if plasticity within cortical fields corresponding to spared modalities, particularly primary sensory cortices, may also contribute. Here, we demonstrate empirically that early loss of vision alters coding of sensory inputs in primary somatosensory cortex in a manner that supports enhanced tactile discrimination.

Alterations in cortical and thalamic connections of somatosensory cortex following early loss of vision

“…The goal of this study was to examine and quantify the effects of early bilateral enucleation on corticocortical and thalamocortical connections of the primary somatosensory cortex (S1) in short-tailed opossums and to compare these to connections of S1 in sighted opossums (Dooley et al, 2013(Dooley et al, , 2015. The present investigation was prompted by the finding that following very early enucleation, the primary somatosensory cortex increases in size (Karlen et al, 2006), neurons in S1 respond to both somatosensory and auditory stimulation (Kahn & Krubitzer, 2002;Karlen et al, 2006) and the neural response properties and receptive field size are altered compared to sighted controls (Ramamurthy & Krubitzer, 2018; Figure 1). Here, we provide anatomical evidence for both novel corticocortical projections, as well FIGURE 8 Location of retrogradely labeled neurons in the thalamus resulting from an injection of CTB in S1.…”

“…In most of the animals examined using neurophysiological mapping techniques, both auditory and somatosensory cortex were reorganized as well. Bottom figures are adapted from Kahn and Krubitzer (2002) and Karlen et al (2006) (Ramamurthy & Krubitzer, 2018). Although it is likely that these functional alterations in S1 are the result of altered connectivity at multiple levels of the nervous system, there are no studies that examine the connections of the primary somatosensory cortex following early loss of vision.…”

“…In early bilaterally enucleated opossums we demonstrated that unlike sighted animals, the primary somatosensory area had a large percentage of recording sites in which neurons responded to both somatosensory and auditory stimulation (Kahn & Krubitzer, ; Karlen et al, ; Figure b). Further, recent work in our laboratory characterizes these functional changes in S1; the receptive fields of neurons were smaller and the ability of individual neurons to detect single whisker stimulation was increased (Ramamurthy & Krubitzer, ). Although it is likely that these functional alterations in S1 are the result of altered connectivity at multiple levels of the nervous system, there are no studies that examine the connections of the primary somatosensory cortex following early loss of vision.…”

Performance and behavioral flexibility on a complex motor task depend on available sensory inputs in early blind and sighted short-tailed opossums

“…Work from our laboratory has recently shown that neurons in the whisker representation of S1 have smaller receptive fields and increased selectivity (i.e. greater discriminability) (Ramamurthy & Krubitzer, 2018). Thus, we sought to examine the role of the whiskers during variable ladder rung walking.…”

“…Similar to rodents, neurons in the reorganized visual cortex of early blind opossums respond instead to deflections of the whiskers and broadband auditory clicks (Karlen et al, 2006). The spared sensory systems are also affected, as early blind opossums exhibit changes in the cortical connections of S1, as well as changes in receptive field size and response properties of neurons in the whisker representation of S1 (Dooley & Krubitzer, 2019;Ramamurthy & Krubitzer, 2018).…”