Lifelong learning: ocular dominance plasticity in mouse visual cortex

Ocular dominance plasticity has long served as a successful model for examining how cortical circuits are shaped by experience. In this paradigm, altered retinal activity caused by unilateral eye-lid closure leads to dramatic shifts in the binocular response properties of neurons in the visual cortex. Much of the recent progress in identifying the cellular and molecular mechanisms underlying ocular dominance plasticity has been achieved by using the mouse as a model system. In this species, monocular deprivation initiated in adulthood also causes robust ocular dominance shifts. Research on ocular dominance plasticity in the mouse is starting to provide insight into which factors mediate and influence cortical plasticity in juvenile and adult animals.     

Distributed neural plasticity for shape learning in the human visual cortex

Expertise in recognizing objects in cluttered scenes is a critical skill for our interactions in complex environments and is thought to develop with learning. However, the neural implementation of object learning across stages of visual analysis in the human brain remains largely unknown. Using combined psychophysics and functional magnetic resonance imaging (fMRI), we show a link between shape-specific learning in cluttered scenes and distributed neuronal plasticity in the human visual cortex. We report stronger fMRI responses for trained than untrained shapes across early and higher visual areas when observers learned to detect low-salience shapes in noisy backgrounds. However, training with high-salience pop-out targets resulted in lower fMRI responses for trained than untrained shapes in higher occipitotemporal areas. These findings suggest that learning of camouflaged shapes is mediated by increasing neural sensitivity across visual areas to bolster target segmentation and feature integration. In contrast, learning of prominent pop-out shapes is mediated by associations at higher occipitotemporal areas that support sparser coding of the critical features for target recognition. We propose that the human brain learns novel objects in complex scenes by reorganizing shape processing across visual areas, while taking advantage of natural image correlations that determine the distinctiveness of target shapes.     

Experience-dependent plasticity in adult visual cortex

Experience-dependent plasticity is a prominent feature of the mammalian visual cortex. Although such neural changes are most evident during development, adult cortical circuits can be modified by a variety of manipulations, such as perceptual learning and visual deprivation. Elucidating the underlying mechanisms at the cellular and synaptic levels is an essential step in understanding neural plasticity in the mature animal. Although developmental and adult plasticity share many common features, notable differences may be attributed to developmental cortical changes at multiple levels. These range from shifts in the molecular profiles of cortical neurons to changes in the spatiotemporal dynamics of network activity. In this review, we will discuss recent progress and remaining challenges in understanding adult visual plasticity, focusing on the primary visual cortex.     

Learning and neural plasticity in visual object recognition

The capability of the adult primate visual system for rapid and accurate recognition of targets in cluttered, natural scenes far surpasses the abilities of state-of-the-art artificial vision systems. Understanding this capability remains a fundamental challenge in visual neuroscience. Recent experimental evidence suggests that adaptive coding strategies facilitated by underlying neural plasticity enable the adult brain to learn from visual experience and shape its ability to integrate and recognize coherent visual objects.     

Cortisol reduces plasticity in the kitten visual cortex

We investigated the effect of elevated levels of cortisol on plasticity in the visual cortex of the cat. Animals were given daily injections of cortisol i.m. for 20 days starting around 35 days of age. After 10 days they were monocularly deprived, and after an additional 10 days recordings were made from the visual cortex to construct an ocular dominance histogram. The results were compared with those from normal animals of the same age, and with animals monocularly deprived for the same period but not treated with cortisol. Cortisol reduced the ocular dominance shift in a dose-dependent manner, but did not totally abolish it even at the highest doses used. Two other series of animals were recorded, one slightly later in the critical period and one slightly earlier, with care taken to give cortisol before the animals were exposed to light in the morning. In both cases, cortisol reduced the ocular dominance shift but did not abolish it. To interpret these results, we measured levels of plasma cortisol in normal cats of various ages. Average levels were fairly constant between birth and 12 months of age (0.5–1 μg/dl), and increased slightly after that, but there was a large variation between animals. Thus elevated levels of cortisol can have a substantial effect on plasticity in the visual cortex of the cat, but the decline of the critical period for plasticity between 6 weeks and 3–5 months of age does not seem to be due to a rise in cortisol levels during this time.     

A precritical period for plasticity in visual cortex

One of the seminal discoveries in developmental neuroscience is that altering visual experience through monocular deprivation can alter both the physiological and the anatomical representation of the two eyes, called ocular dominance columns, in primary visual cortex. This rearrangement is restricted to a critical period that starts a few days or weeks after vision is established and ends before adulthood. In contrast to the original hypothesis proposed by Hubel and Wiesel, ocular dominance columns are already substantially formed before the onset of the critical period. Indeed, before the critical period there is a period of ocular dominance column formation during which there is robust spontaneous activity and visual experience. Recent findings raise important questions about whether activity guides ocular dominance column formation in this 'precritical period'. One developmental event that marks the passage from the precritical period to the critical period is the activation of a GABAergic circuit. How these events trigger the transition from the precritical to critical period is not known.     

Simulation of plasticity in the adult visual cortex

 Retinal plasticity has been shown in the adult visual nervous system in mammals. Following a retinal lesion (scotoma) there is a reorganization of the cortical receptive field distribution: cortical neurons selective to visual stimuli in the area of the visual field corresponding to the retinal lesion, become selective to other parts of the visual field. In this work, we study this effect with a self-organizing neural network. In a first stage, the network reaches a pattern of connectivity that represents normal development of neuronal selectivity. The scotoma is simulated by perturbing accordingly the properties of a region of the input layer representing the retina. The system evolves to a new receptive field distribution mainly by means of the reorganization of the intra cortical connectivity. No major change of the geniculo cortical connectivity is detected. This may explain the surprisingly short time scale of the event. Received: 6 June 2000 / Accepted in revised form: 16 October 2000     

Sleep enhances plasticity in the developing visual cortex

During a critical period of brain development, occluding the vision of one eye causes a rapid remodeling of the visual cortex and its inputs. Sleep has been linked to other processes thought to depend on synaptic remodeling, but a role for sleep in this form of cortical plasticity has not been demonstrated. We found that sleep enhanced the effects of a preceding period of monocular deprivation on visual cortical responses, but wakefulness in complete darkness did not do so. The enhancement of plasticity by sleep was at least as great as that produced by an equal amount of additional deprivation. These findings demonstrate that sleep and sleep loss modify experience-dependent cortical plasticity in vivo. They suggest that sleep in early life may play a crucial role in brain development.     

Molecular mechanisms of experience-dependent plasticity in visual cortex

A remarkable amount of our current knowledge of mechanisms underlying experience-dependent plasticity during cortical development comes from study of the mammalian visual cortex. Recent advances in high-resolution cellular imaging, combined with genetic manipulations in mice, novel fluorescent recombinant probes, and large-scale screens of gene expression, have revealed multiple molecular mechanisms that underlie structural and functional plasticity in visual cortex. We situate these mechanisms in the context of a new conceptual framework of feed-forward and feedback regulation for understanding how neurons of the visual cortex reorganize their connections in response to changes in sensory inputs. Such conceptual advances have important implications for understanding not only normal development but also pathological conditions that afflict the central nervous system.     

Fragment-based learning of visual object categories

When we perceive a visual object, we implicitly or explicitly associate it with a category we know. It is known that the visual system can use local, informative image fragments of a given object, rather than the whole object, to classify it into a familiar category. How we acquire informative fragments has remained unclear. Here, we show that human observers acquire informative fragments during the initial learning of categories. We created new, but naturalistic, classes of visual objects by using a novel "virtual phylogenesis" (VP) algorithm that simulates key aspects of how biological categories evolve. Subjects were trained to distinguish two of these classes by using whole exemplar objects, not fragments. We hypothesized that if the visual system learns informative object fragments during category learning, then subjects must be able to perform the newly learned categorization by using only the fragments as opposed to whole objects. We found that subjects were able to successfully perform the classification task by using each of the informative fragments by itself, but not by using any of the comparable, but uninformative, fragments. Our results not only reveal that novel categories can be learned by discovering informative fragments but also introduce and illustrate the use of VP as a versatile tool for category-learning research.     

条件性运动学习的神经基础

人和动物形成多样的、快速可变的刺激－反应联合关系的过程被称为条件性运动学习。条件性运动学习使得人和动物具有很强的适应优势。损毁或行为电生理研究表明：运动前区背外侧部、基底神经节以及前额叶皮层腹侧部在条件性运动学习中起至关重要的作用;海马在条件性运动学习中也起着一定的作用;而杏仁核等一些结构在条件性运动学习中不起作用。     

On perceptual analyzers underlying visual texture discrimination: Part II

In Part I Caelli and Julesz generated texture pairs of 4-disk micropatterns with identical dipole statistics. They found that this iso-dipole constraint could not prevent the quasi-collinearity of certain disk elements which, in turn, yielded effortless discrimination. They proposed two classes of perceptual analyzers to explain discrimination with these micropatern textures: Class A, corresponding to those which detect dipole differences; while Class B detectors, such as the quasi-collinear detector (QCD), acted when isodipole textures were presented. In this paper we show several new methods for generating iso-dipole textures with micropatterns consisting of 5 or more disks or non-disk shaped elements, and we report the discovery of two other Class B detectors, a corner detector (using a 6-disk method), and a closure detector (with 8–11 disk micropatterns). These QCD, corner, and closure detectors were verified by examining several hundred iso-dipole texture pairs. It appears that iso-dipole constraints make ineffective all other feature analyzers involved in effortless texture discrimination than the Class B types. These figural properties of collinearity, corners, and closure can be perceived without scrutiny and are precursors of form perception.     

On perceptual analyzers underlying visual texture discrimination: Part I

We have found a class of feature detectors, based on the quasi-collinearity of dots, which result in visual texture discrimination even when second order statistics are equal. This degenerate counterexample to the Julesz conjecture on effortless texture discrimination has supplied the key to a simple theory of texture discrimination. Accordingly, effortless texture discrimination is based on two classses of perceptual detectors: Class A, those that measure differences in second-order (dipole) statistics; Class B, those that can still detect statistical differences in some features when second-order statistics are kept identical; for instance, the quasi-collinearity of adjacent dipoles. The difference thresholds (tuning curves) for the perceptual dipole and quasi-collinearity detectors have been determined. These texture pairs were generated by a method that creates micropatterns with iso-dipole duals from 4 disks. The extension of this 4-disk method to 5 and more disks with iso-dipole duals permits the search for other kinds of perceptual detectors and will be discussed in Part II.     

NMDA receptor-dependent ocular dominance plasticity in adult visual cortex

The binocular region of mouse visual cortex is strongly dominated by inputs from the contralateral eye. Here we show in adult mice that depriving the dominant contralateral eye of vision leads to a persistent, NMDA receptor-dependent enhancement of the weak ipsilateral-eye inputs. These data provide in vivo evidence for metaplasticity as a mechanism for binocular competition and demonstrate that an ocular dominance shift can occur solely by the mechanisms of response enhancement. They also show that adult mouse visual cortex has a far greater potential for experience-dependent plasticity than previously appreciated. These insights may force a revision in how data on ocular dominance plasticity in mutant mice have been interpreted.     

Adaptation-induced plasticity of orientation tuning in adult visual cortex

A key emergent property of the primary visual cortex (V1) is the orientation selectivity of its neurons. The extent to which adult visual cortical neurons can exhibit changes in orientation selectivity is unknown. Here we use single-unit recording and intrinsic signal imaging in V1 of adult cats to demonstrate systematic repulsive shifts in orientation preference following short-term exposure (adaptation) to one stimulus orientation. In contrast to the common view of adaptation as a passive process by which responses around the adapting orientation are reduced, we show that changes in orientation tuning also occur due to response increases at orientations away from the adapting stimulus. Adaptation-induced orientation plasticity is thus an active time-dependent process that involves network interactions and includes both response depression and enhancement.     

Cortisol reduces plasticity in the kitten visual cortex.

We investigated the effect of elevated levels of cortisol on plasticity in the visual cortex of the cat. Animals were given daily injections of cortisol i.m. for 20 days starting around 35 days of age. After 10 days they were monocularly deprived, and after an additional 10 days recordings were made from the visual cortex to construct an ocular dominance histogram. The results were compared with those from normal animals of the same age, and with animals monocularly deprived for the same period but not treated with cortisol. Cortisol reduced the ocular dominance shift in a dose-dependent manner, but did not totally abolish it even at the highest doses used. Two other series of animals were recorded, one slightly later in the critical period and one slightly earlier, with care taken to give cortisol before the animals were exposed to light in the morning. In both cases, cortisol reduced the ocular dominance shift but did not abolish it. To interpret these results, we measured levels of plasma cortisol in normal cats of various ages. Average levels were fairly constant between birth and 12 months of age (0.5-1 microgram/dl), and increased slightly after that, but there was a large variation between animals. Thus elevated levels of cortisol can have a substantial effect on plasticity in the visual cortex of the cat, but the decline of the critical period for plasticity between 6 weeks and 3-5 months of age does not seem to be due to a rise in cortisol levels during this time.     

Genetic control of experience-dependent plasticity in the visual cortex

Depriving one eye of visual experience during a sensitive period of development results in a shift in ocular dominance (OD) in the primary visual cortex (V1). To assess the heritability of this form of cortical plasticity and identify the responsible gene loci, we studied the influence of monocular deprivation on OD in a large number of recombinant inbred mouse strains derived from mixed C57BL/6J and DBA/2J backgrounds (BXD). The strength of imaged intrinsic signal responses in V1 to visual stimuli was strongly heritable as were various elements of OD plasticity. This has important implications for the use of mice of mixed genetic backgrounds for studying OD plasticity. C57BL/6J showed the most significant shift in OD, while some BXD strains did not show any shift at all. Interestingly, the increase in undeprived ipsilateral eye responses was not correlated to the decrease in deprived contralateral eye responses, suggesting that the size of these components of OD plasticity are not genetically controlled by only a single mechanism. We identified a quantitative trait locus regulating the change in response to the deprived eye. The locus encompasses 13 genes, two of which--Stch and Nrip1--contain missense polymorphisms. The expression levels of Stch and to a lesser extent Nrip1 in whole brain correlate with the trait identifying them as novel candidate plasticity genes.