Cortical feedback modulates distinct critical period development in mouse visual thalamus.
Ontology highlight
ABSTRACT:
SUBMITTER: Li N
PROVIDER: S-EPMC9794980 | biostudies-literature | 2023 Jan
REPOSITORIES: biostudies-literature
Publications
Cortical feedback modulates distinct critical period development in mouse visual thalamus.
Li Na N Liu Qiong Q Zhang Yimu Y Yang Zhongyi Z Shi Xuefeng X Gu Yu Y
iScience 20221207 1
In primary visual cortex (V1), critical period for ocular dominance (OD) plasticity is a well-defined developmental stage to shape neuronal circuits based on visual experience. Recent studies showed that V1-like OD plasticity existed in mouse dorsal lateral geniculate nucleus (dLGN). It is still unclear what the exact time window is and how neural circuits contribute to OD plasticity in dLGN. Using <i>in vivo</i> electrophysiology, we defined a critical period for OD plasticity in dLGN from eye ...[more]
Similar Datasets
Project description:Study of the neural deficits caused by mismatched binocular vision in early childhood has predominantly focused on circuits in the primary visual cortex (V1). Recent evidence has revealed that neurons in mouse dorsolateral geniculate nucleus (dLGN) can undergo rapid ocular dominance plasticity following monocular deprivation (MD). It remains unclear, however, whether the long-lasting deficits attributed to MD during the critical period originate in the thalamus. Using in vivo two-photon Ca2+ imaging of dLGN afferents in superficial layers of V1 in female and male mice, we demonstrate that 14 d MD during the critical period leads to a chronic loss of binocular dLGN inputs while sparing response strength and spatial acuity. Importantly, MD leads to profoundly mismatched visual tuning properties in remaining binocular dLGN afferents. Furthermore, MD impairs binocular modulation, reducing facilitation of responses of both binocular and monocular dLGN inputs during binocular viewing. As predicted by our findings in thalamic inputs, Ca2+ imaging from V1 neurons revealed spared spatial acuity but impaired binocularity in L4 neurons. V1 L2/3 neurons in contrast displayed deficits in both binocularity and spatial acuity. Our data demonstrate that critical-period MD produces long-lasting disruptions in binocular integration beginning in early binocular circuits in dLGN, whereas spatial acuity deficits first arise from circuits further downstream in V1. Our findings indicate that the development of normal binocular vision and spatial acuity depend upon experience-dependent refinement of distinct stages in the mammalian visual system.SIGNIFICANCE STATEMENT Abnormal binocular vision and reduced acuity are hallmarks of amblyopia, a disorder that affects 2%-5% of the population. It is widely thought that the neural deficits underlying amblyopia begin in the circuits of primary visual cortex. Using in vivo two-photon calcium imaging of thalamocortical axons in mice, we show that depriving one eye of input during a critical period in development chronically impairs binocular integration in thalamic inputs to primary visual cortex. In contrast, visual acuity is spared in thalamic inputs. These findings shed new light on the role for developmental mechanisms in the thalamus in establishing binocular vision and may have critical implications for amblyopia.
| S-EPMC6961993 | biostudies-literature
Project description:The mouse dorsal lateral geniculate nucleus (dLGN) is an intermediary between retina and primary visual cortex (V1). Recent investigations are beginning to reveal regional complexity in mouse dLGN. Using local injections of retrograde tracers into V1 of adult and neonatal mice, we examined the developing organisation of geniculate projection columns: the population of dLGN-V1 projection neurons that converge in cortex. Serial sectioning of the dLGN enabled the distribution of labelled projection neurons to be reconstructed and collated within a common standardised space. This enabled us to determine: the organisation of cells within the dLGN-V1 projection columns; their internal organisation (topology); and their order relative to V1 (topography). Here, we report parameters of projection columns that are highly variable in young animals and refined in the adult, exhibiting profiles consistent with shell and core zones of the dLGN. Additionally, such profiles are disrupted in adult animals with reduced correlated spontaneous activity during development. Assessing the variability between groups with partial least squares regression suggests that 4-6 cryptic lamina may exist along the length of the projection column. Our findings further spotlight the diversity of the mouse dLGN--an increasingly important model system for understanding the pre-cortical organisation and processing of visual information. Furthermore, our approach of using standardised spaces and pooling information across many animals will enhance future functional studies of the dLGN.
| S-EPMC4699701 | biostudies-literature
Project description:The visual system is composed of diverse cell types that encode distinct aspects of the visual scene and may form separate processing channels. Here we present further evidence for that hypothesis whereby functional cell groups in the dorsal lateral geniculate nucleus (dLGN) are differentially modulated during behavior. Using simultaneous multi-electrode recordings in dLGN and primary visual cortex (V1) of behaving mice, we characterized the impact of locomotor activity on response amplitude, variability, correlation and spatiotemporal tuning. Locomotion strongly impacts the amplitudes of dLGN and V1 responses but the effects on variability and correlations are relatively minor. With regards to tunings, locomotion enhances dLGN responses to high temporal frequencies, preferentially affecting ON transient cells and neurons with nonlinear responses to high spatial frequencies. Channel specific modulations may serve to highlight particular visual inputs during active behaviors.
| S-EPMC6242985 | biostudies-literature
Project description:In contrast to the prenatal development of the cerebral cortex, when cell production, migration, and layer formation dominate, development after birth involves more subtle processes, such as activity-dependent plasticity that includes refinement of synaptic connectivity by its stabilization and elimination. In the present study, we use RNA-seq with high spatial resolution to examine differential gene expression across layers 2/3, 4, 5, and 6 of the mouse visual cortex before the onset of the critical period of plasticity [postnatal day 5 (P5)], at its peak (P26), and at the mature stage (P180) and compare it with the prefrontal association area. We find that, although genes involved in early developmental events such as cell division, neuronal migration, and axon guidance are still prominent at P5, their expression largely terminates by P26, when synaptic plasticity and associated signaling pathways become enriched. Unexpectedly, the gene expression profile was similar in both areas at this age, suggesting that activity-dependent plasticity between visual and association cortices are subject to the same genetic constraints. Although gene expression changes follow similar paths until P26, we have identified 30 regionally enriched genes that are prominent during the critical period. At P180, we identified several hundred differentially expressed gene isoforms despite subsiding levels of gene expression differences. This result indicates that, once genetic developmental programs cease, the remaining morphogenetic processes may depend on posttranslational events.
| S-EPMC4491803 | biostudies-literature
Project description:Visual information is detected by the retina and transmitted into the brain by retinal ganglion cells. In rodents, the visual thalamus is a major recipient of retinal ganglion cells axons and is divided into three functionally distinct nuclei: the dorsal lateral geniculate nucleus (dLGN), ventral LGN (vLGN), and intergeniculate leaflet. Despite being densely innervated by retinal input, each nucleus in rodent visual thalamus possesses diverse molecular profiles which underpin their unique circuitry and cytoarchitecture. Here, we combined large-scale unbiased proteomic and transcriptomic analyses to elucidate the molecular expression profiles of the developing mouse dLGN and vLGN. We identified several extracellular matrix proteins as differentially expressed in these regions, particularly constituent molecules of perineuronal nets (PNNs). Remarkably, we discovered at least two types of molecularly distinct Aggrecan-rich PNN populations in vLGN, exhibiting non-overlapping spatial, temporal, and cell-type specific expression patterns. The mechanisms responsible for the formation of these two populations of PNNs also differ as the formation of Cat315+ PNNs (but not WFA+ PNNs) required input from the retina. This study is first to suggest that cell type- and molecularly specific supramolecular assemblies of extracellular matrix may play important roles in the circuitry associated with the subcortical visual system and in the processing of visual information. OPEN SCIENCE BADGES: This article has received a badge for *Open Materials* because it provided all relevant information to reproduce the study in the manuscript. The complete Open Science Disclosure form for this article can be found at the end of the article. More information about the Open Practices badges can be found at https://cos.io/our-services/open-science-badges/. Cover Image for this issue: doi: 10.1111/jnc.14203.
| S-EPMC6532419 | biostudies-literature
Project description:In an ever-changing environment, crossmodal recalibration is crucial to maintain precise and coherent spatial estimates across different sensory modalities. Accordingly, it has been found that perceived auditory space is recalibrated toward vision after consistent exposure to spatially misaligned audio-visual stimuli (VS). While this so-called ventriloquism aftereffect (VAE) yields internal consistency between vision and audition, it does not necessarily lead to consistency between the perceptual representation of space and the actual environment. For this purpose, feedback about the true state of the external world might be necessary. Here, we tested whether the size of the VAE is modulated by external feedback and reward. During adaptation audio-VS with a fixed spatial discrepancy were presented. Participants had to localize the sound and received feedback about the magnitude of their localization error. In half of the sessions the feedback was based on the position of the VS and in the other half it was based on the position of the auditory stimulus. An additional monetary reward was given if the localization error fell below a certain threshold that was based on participants' performance in the pretest. As expected, when error feedback was based on the position of the VS, auditory localization during adaptation trials shifted toward the position of the VS. Conversely, feedback based on the position of the auditory stimuli reduced the visual influence on auditory localization (i.e., the ventriloquism effect) and improved sound localization accuracy. After adaptation with error feedback based on the VS position, a typical auditory VAE (but no visual aftereffect) was observed in subsequent unimodal localization tests. By contrast, when feedback was based on the position of the auditory stimuli during adaptation, no auditory VAE was observed in subsequent unimodal auditory trials. Importantly, in this situation no visual aftereffect was found either. As feedback did not change the physical attributes of the audio-visual stimulation during adaptation, the present findings suggest that crossmodal recalibration is subject to top-down influences. Such top-down influences might help prevent miscalibration of audition toward conflicting visual stimulation in situations in which external feedback indicates that visual information is inaccurate.
| S-EPMC6979315 | biostudies-literature
Project description:Nociceptive signals are usually transmitted to layer 4 neurons in somatosensory cortex via the spinothalamic-thalamocortical pathway. The layer 5 corticospinal neurons in sensorimotor cortex are reported to receive the output of neurons in superficial layers; and their descending axons innervate the spinal cord to regulate basic sensorimotor functions. Here, we show that a subset of layer 5 neurons receives spinal inputs through a direct spino-cortical circuit bypassing the thalamus, and thus define these neurons as spino-cortical recipient neurons (SCRNs). Morphological studies revealed that the branches from spinal ascending axons formed a kind of disciform structure with the descending axons from SCRNs in the basilar pontine nucleus (BPN). Electron microscopy and calcium imaging further confirmed that the axon terminals from spinal ascending neurons and SCRNs made functional synaptic contacts in the BPN, linking the ascending sensory pathway to the descending motor control pathway. Furthermore, behavioral tests indicated that the spino-cortical connection in the BPN was involved in nociceptive responses. In vivo calcium imaging showed that SCRNs responded to peripheral noxious stimuli faster than neighboring layer 4 cortical neurons in awake mice. Manipulating activities of SCRNs could modulate nociceptive behaviors. Therefore, this direct spino-cortical circuit represents a noncanonical pathway, allowing a fast sensory-motor transition of the brain in response to noxious stimuli.
| S-EPMC10542357 | biostudies-literature
Project description:Circadian rhythms control a variety of physiological processes, but whether they may also time brain development remains largely unknown. Here, we show that circadian clock genes control the onset of critical period plasticity in the neocortex. Within visual cortex of Clock-deficient mice, the emergence of circadian gene expression was dampened, and the maturation of inhibitory parvalbumin (PV) cell networks slowed. Loss of visual acuity in response to brief monocular deprivation was concomitantly delayed and rescued by direct enhancement of GABAergic transmission. Conditional deletion of Clock or Bmal1 only within PV cells recapitulated the results of total Clock-deficient mice. Unique downstream gene sets controlling synaptic events and cellular homeostasis for proper maturation and maintenance were found to be mis-regulated by Clock deletion specifically within PV cells. These data demonstrate a developmental role for circadian clock genes outside the suprachiasmatic nucleus, which may contribute mis-timed brain plasticity in associated mental disorders.
| S-EPMC4392344 | biostudies-literature
Project description:In an attempt to chart parallel sensory streams passing through the visual thalamus, we acquired a 100-trillion-voxel electron microscopy (EM) dataset and identified cohorts of retinal ganglion cell axons (RGCs) that innervated each of a diverse group of postsynaptic thalamocortical neurons (TCs). Tracing branches of these axons revealed the set of TCs innervated by each RGC cohort. Instead of finding separate sensory pathways, we found a single large network that could not be easily subdivided because individual RGCs innervated different kinds of TCs and different kinds of RGCs co-innervated individual TCs. We did find conspicuous network subdivisions organized on the basis of dendritic rather than neuronal properties. This work argues that, in the thalamus, neural circuits are not based on a canonical set of connections between intrinsically different neuronal types but, rather, may arise by experience-based mixing of different kinds of inputs onto individual postsynaptic cells.
| S-EPMC4808248 | biostudies-literature
Project description:Sensory microcircuits are refined by experience during windows of heightened plasticity termed "critical periods" (CPs). In visual cortex the effects of visual deprivation change dramatically at the transition from the pre-CP to the CP, but the cellular plasticity mechanisms that underlie this change are poorly understood. Here we show that plasticity at unitary connections between GABAergic Fast Spiking (FS) cells and Star Pyramidal (SP) neurons within layer 4 flips sign at the transition between the pre-CP and the CP. During the pre-CP, coupling FS firing with SP depolarization induces long-term depression of inhibition at this synapse, whereas the same protocol induces long-term potentiation of inhibition at the opening of the CP. Despite being of opposite sign, both forms of plasticity share expression characteristics--a change in coefficient of variation with no change in paired-pulse ratio--and depend on GABAB receptor signaling. Finally, we show that the reciprocal SP → FS synapse also acquires the ability to undergo long-term potentiation at the pre-CP to CP transition. Thus, at the opening of the CP, there are coordinated changes in plasticity that allow specific patterns of activity within layer 4 to potentiate feedback inhibition by boosting the strength of FS ↔ SP connections.
| S-EPMC3839695 | biostudies-other