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Pallas, S. L.

Publications and source records attributed to Pallas, S. L..

5 recordsLinked to original sources

Refinement and maintenance of receptive field size in primary visual cortex occurs without visual experience in mice

A critical step in visual cortical maturation is refinement of receptive field (RF) size, producing higher acuity vision. This was previously studied using species with well-developed vision (e.g., carnivores, primates), in which visual experience was necessary for refinement but not maintenance of RFs in visual cortex. In contrast, in Syrian hamsters, a crepuscular species with low visual acuity, dark rearing had no effect on RF refinement in juveniles, but RFs re-enlarged in adulthood, resulting in reduced acuity. These inter-species differences raise the question of whether the need for visual experience is primarily related to the phylogenetic position of the species or to its ecological niche. Here we report that dark rearing had no effect on development or maintenance of RF properties of visual cortical neurons in nocturnal mice. Mice with lifelong visual deprivation refined and maintained their RF size over time. Furthermore, the development of stimulus direction tuning was unaffected by dark rearing. In contrast, surround suppression, orientation tuning and the sharpness of direction tuning were abnormal in dark reared mice. These and our previous results from hamsters show that species living in an ecological niche with minimal daylight exposure require little to no visual experience to develop and maintain refined RFs. This study is an important step in developing a better understanding of the role of visual experience in the development of visual processing circuitry and suggests that diurnal mammals may be a better model for human visual cortical development than mice. SIGNIFICANCE STATEMENTThe role of visual experience in development and plasticity of receptive fields in visual cortex was initially studied using animals with well-developed visual systems (carnivores, primates). Mice have been used more recently, primarily because of genetic manipulations. Now that gene alteration is possible in other species, whether mice are the best choice for visual development and plasticity studies needs reevaluation. We assayed the role of visual experience in mouse visual cortical development, focusing on receptive field refinement. We report that visual experience is unnecessary for the refinement of receptive fields in visual cortex, suggesting that mice (Mus musculus) may not be the best animal model to demonstrate how visual experience influences the development of visual cortical circuitry in humans.

neuroscience↗

Chilean brush tailed mouse (Octodon degus): a diurnal precocial rodent as a new model to study visual receptive field properties of superior colliculus neurons

Lab rodent species used to study the visual system and its development (hamsters, rats, and mice) are nocturnal, altricial, and possess simpler visual systems than carnivores and primates. To widen the spectra of studied species, here we introduce an alternative model, the Chilean degu (Octodon degus), a diurnal, precocial Caviomorph rodent with a cone enriched, well-structured retina, and well-developed central visual projections. To assess degus visual physiological properties, we characterized the visual responses and receptive field (RF) properties of isolated neurons in the superficial layers of the superior colliculus (sSC). To facilitate comparison with studies in other rodent species, we used four types of stimuli: (1) a moving white square, (2) sinusoidal gratings, (3) an expanding black circle (looming), and (4) a stationary black circle. We found that as in other mammalian species, RF size increases from superficial to deeper SC layers. Interestingly, compared to other lab rodents, degus have smaller RF sizes, likely indicating higher acuity. sSC neurons displayed spatial frequency tuning to grating stimuli from 0.08 to 0.24 cycles/degree. Additionally, neurons from sSC showed transient ON, OFF, or ON-OFF responses to stationary stimuli but increased their firing rates as a looming object increased in size. Our results suggests that degus have higher visual acuity, higher frequency tuning, and lower contrast sensitivity than commonly used nocturnal lab rodents, positioning degus as a well-suited model for studies of diurnal vision that are more relevant to humans.

neuroscience↗

Multiple Postsynaptic Protein Levels Are Maintained in a Delayed Form of Compensatory, Experience-Dependent Plasticity in Adult Superior Colliculus

Visual deprivation by dark rearing in kittens and monkeys delays visual pathway development and prolongs the critical period. In contrast, receptive fields (RFs) in superior colliculus (SC) of Syrian hamsters (Mesocricetus auratus) refine normally with spontaneous activity alone, requiring only brief juvenile visual experience to maintain refined RFs in adulthood (Carrasco et al., 2005). Extending dark rearing past puberty leads to lower GAD and GABA levels due to reduced BDNF-TrkB signaling, resulting in RF re-enlargement (Carrasco et al., 2011; Mudd et al., 2019). Previous studies in kittens and monkeys have reported that dark rearing is associated with changes in both GABA ligand and GABAA receptor levels. Given the reduced GABA levels in SC of dark reared adult hamsters, we asked if dark rearing also causes changes in GABAA receptor levels. We examined expression of GABAA receptor subunits, their anchoring protein gephyrin, and the cation-chloride co-transporters KCC2 and NKCC1 in dark reared hamsters. Surprisingly, we found that dark rearing from birth until puberty had no effect on the levels of any of these postsynaptic elements, revealing a new form of maladaptive, presynaptic only inhibitory plasticity in which, rather than extending the critical period as seen in kittens and monkeys, hamster receptive fields refine normally and then lose refinement in adulthood. These results suggest that attempts to increase plasticity in adulthood for rehabilitation or recovery from injury should consider the possibility of unintended negative consequences. In addition, our results demonstrate the interesting finding that changes in neurotransmitter levels are not necessarily coordinated with changes in postsynaptic components.

neuroscience↗

Dynamic alterations of retinal EphA5 expression in retinocollicular map plasticity

The topographically ordered retinocollicular projection is an excellent system for studying the mechanism of axon guidance. Gradients of EphA receptors in the retina and ephrin-As in the superior colliculus (SC) pattern the anteroposterior axis of the retinocollicular map, but whether they are involved in map plasticity after injury is unknown. Partial damage to the caudal SC at birth creates a compressed, complete retinotopic map in the remaining SC without affecting visual response properties. Previously, we found that the gradient of ephrinA expression in compressed maps is steeper than normal, suggesting an instructive role in compression (Tadesse et al., 2013). Here we measured EphA5 mRNA and protein levels after caudal SC damage in order to test the hypothesis that changes in retinal EphA5 expression occur that are complementary to the changes in collicular ephrin-A expression. We find that the nasotemporal gradient of EphA5 receptor expression steepens in the retina and overall expression levels change dynamically, especially in temporal retina, supporting the hypothesis. This change in receptor expression occurs after the change in ephrin-A ligand expression. We propose that changes in the retinal EphA5 gradient guide recovery of the retinocollicular projection from early injury. This could occur directly through the change in EphA5 expression instructing retino-SC map compression, or through ephrinA ligand signaling instructing a change in EphA5 receptor expression that in turn signals the retinocollicular map to compress. Understanding what molecular signals direct compensation for injury is essential to developing rehabilitative strategies and maximizing the potential for recovery.

neuroscience↗

TrkB activation during a critical period mimics the protective effects of early visual experience on the stability of receptive fields in adult superior colliculus

During a critical period in postnatal development, spontaneous and evoked retinal activity shape nascent visual pathways in an adaptive fashion. Visual experience increases transcription of the neurotrophin BDNF, activating the BDNF receptor TrkB, which promotes maturation of parvalbumin (PV) positive inhibitory interneurons, a process thought to open a critical period for ocular dominance plasticity in visual cortex. Development of perineuronal nets around PV neurons limits plasticity, ending the critical period and restricting adult plasticity. Another form of critical period plasticity is receptive field (RF) refinement. Spontaneous activity alone is sufficient for spatial refinement of visual receptive fields in superior colliculus (SC) and visual cortex (V1), but visual experience during an early critical period is necessary to maintain inhibitory synapses and stabilize RFs in adulthood (Carrasco et al. 2005, 2011; Carrasco & Pallas 2006; Balmer & Pallas 2015a). We report here that deprivation-induced RF enlargement in adulthood has a behavioral consequence; it impairs fear responses to looming objects in mice and hamsters. The mechanism through which early experience protects RFs from deprivation-induced loss of inhibition in adulthood is unknown. Given that the loss of RF refinement in SC does not occur until adulthood, and that inhibitory PV neurons and perineuronal nets are rare in SC, we asked whether or not BDNF-TrkB signaling was involved. We find that early TrkB activation is necessary and sufficient to maintain visual RF refinement in adulthood, suggesting a common signaling pathway for maturation of inhibition across neuronal subtypes and locations within the visual pathway.\n\nSignificance StatementReceptive field refinement in superior colliculus (SC) differs from more commonly studied examples of critical period plasticity in visual pathways in that it does not require visual experience to occur; rather spontaneous activity is sufficient. Maintenance of refinement requires brief, early exposure to light to stabilize inhibition beyond puberty. This type of inhibitory plasticity must not depend on parvalbumin (PV)-containing GABAergic interneurons or on the formation of perineuronal nets, because these are very uncommon in SC. Nonetheless, we find that TrkB activation during a critical period can substitute for visual experience in maintaining receptive field refinement into adulthood, and that this maintenance is beneficial to visual survival behaviors. Thus, multiple types of plasticity converge on the same neurotrophin-dependent signaling cascade.

neuroscience↗