The evolution of whisker‐mediated somatosensation in mammals: Sensory processing in barrelless S1 cortex of a marsupial, <i>Monodelphis domestica</i>

Ramamurthy, Deepa L.; Krubitzer, Leah

doi:10.1002/cne.24018

Cited by 12 publications

(13 citation statements)

References 95 publications

(164 reference statements)

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“…Interestingly, our findings resemble some forms of plasticity previously reported in the S1 whisker representation, which are functionally distinct from Hebbian forms of plasticity (for review, see Feldman and Brecht, 2005) typically observed in studies involving manipulations that create competition among sensory inputs within the whisker system (e.g., deprivation of a subset of whisker inputs though trimming, plucking, or follicle lesion). Polley et al (2004) found that prolonged exposure of rats to complex, naturalistic environments in adulthood resulted in the contraction of the functional representation of individual whiskers, suppression of whisker-evoked responses, and smaller, sharper receptive fields for neurons in S1. Further, when adult rats were allowed brief periods of whisker-guided exploration in a novel environment after deprivation of all but a single whisker, the direction of Hebbian plasticity was reversed, causing a contraction of the functional representation of the spared whisker rather than its expansion (Polley et al, 1999).…”

Section: Discussionmentioning

confidence: 97%

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

Ramamurthy

Krubitzer

2018

J. Neurosci.

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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.

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Section: Discussionmentioning

confidence: 97%

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

Ramamurthy

Krubitzer

2018

J. Neurosci.

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“…After 4x rinsing in PBS, secondary antibody Alexa Flour 488 goat anti‐Mouse (RRID:AB_2534088; diluted in PBS‐Tx 0.1%) was added for 6 hr at RT. The mouse anti‐Parvalbumin generated against purified frog muscle Parvalbumin is highly specific and recognizes a single band of ∼12 kDa in Western blots of lysed brain tissue, the molecular weight of Parvalbumin (Ramamurthy & Krubitzer, ).…”

Section: Methodsmentioning

confidence: 99%

The centrifugal visual system of a palaeognathous bird, the Chilean Tinamou (Nothoprocta perdicaria)

Krabichler

Vega‐Zuniga

Carrasco

et al. 2017

J of Comparative Neurology

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The avian centrifugal visual system, which projects from the brain to the retina, has been intensively studied in several Neognathous birds that have a distinct isthmo-optic nucleus (ION). However, birds of the order Palaeognathae seem to lack a proper ION in histologically stained brain sections. We had previously reported in the palaeognathous Chilean Tinamou (Nothoprocta perdicaria) that intraocular injections of Cholera Toxin B subunit retrogradely label a considerable number of neurons, which form a diffuse isthmo-optic complex (IOC). In order to better understand how this IOC-based centrifugal visual system is organized, we have studied its major components by means of in vivo and in vitro tracing experiments. Our results show that the IOC, though structurally less organized than an ION, possesses a dense core region consisting of multipolar neurons. It receives afferents from neurons in L10a of the optic tectum, which are distributed with a wider interneuronal spacing than in Neognathae. The tecto-IOC terminals are delicate and divergent, unlike the prominent convergent tecto-ION terminals in Neognathae. The centrifugal IOC terminals in the retina are exclusively divergent, resembling the terminals from "ectopic" centrifugal neurons in Neognathae. We conclude that the Tinamou's IOC participates in a comparable general IOC-retina-TeO-IOC circuitry as the neognathous ION. However, the connections between the components are structurally different and their divergent character suggests a lower spatial resolution. Our findings call for further comparative studies in a broad range of species for advancing our understanding of the evolution, plasticity and functional roles of the avian centrifugal visual system.

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“…In the current study, we examined the role of two sets of facial whiskers -the mystacial whiskers (on the snout) and genal whiskers (on the cheek; Ramamurthy and Krubitzer, 2016) in guiding tactile-based decisions in early blind and sighted opossums, and measured their behavioral discrimination sensitivity to texture cues. To our knowledge, this is the first psychometric investigation of texture discrimination in a marsupial.…”

Section: Introductionmentioning

confidence: 99%

Developmental plasticity of texture discrimination following early vision loss in the marsupialMonodelphis domestica

Ramamurthy

Dodson

Krubitzer³

2020

Preprint

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Behavioral strategies that depend on sensory information are not immutable; rather they can be shaped by the specific sensory context in which animals develop. This behavioral plasticity depends on the remarkable capacity for the brain to reorganize in response to alterations in the sensory environment, particularly when changes in sensory input occur at an early age. To study this phenomenon, we utilize the short-tailed opossum, a marsupial that has been a valuable animal model to study developmental plasticity due to the extremely immature state of its nervous system at birth. Previous studies in opossums have demonstrated that removal of retinal inputs early in development results in profound alterations to cortical connectivity and functional organization of visual and somatosensory cortex; however, behavioral consequences of this plasticity are not well understood. We trained early blind (EB) and sighted control (SC) opossums to perform a two-alternative forced choice texture discrimination task. Whisker trimming caused an acute deficit in discrimination accuracy for both EB and SC animals indicating that they primarily used a whisker-based strategy to guide choices based on tactile cues − though performance recovered in days, suggesting a shift to the use of other body parts when whiskers were absent. Mystacial whiskers were important for performance in both groups; however, genal whiskers only contributed to performance in EB animals. EB opossums significantly outperformed SC opossums in discrimination accuracy, being more sensitive to textural differences by ~75 μm smaller. Our results support behavioral compensation following early blindness using tactile inputs, especially the whisker system.

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The evolution of whisker‐mediated somatosensation in mammals: Sensory processing in barrelless S1 cortex of a marsupial, Monodelphis domestica

Cited by 12 publications

References 95 publications

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

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

The centrifugal visual system of a palaeognathous bird, the Chilean Tinamou (Nothoprocta perdicaria)

Developmental plasticity of texture discrimination following early vision loss in the marsupialMonodelphis domestica

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