Masanobu Miyashita

A mathematical model for the self-organization of orientation columns in visual cortex

The visual cortex contains regular arrangements of neurons responding to specific types of visual stimulation, such as ocular dominance columns and orientation columns. These columnar structures can be considered as the functional architecture for early visual information processing. The model of activity-dependent self-organization reported here demonstrates that both response properties of neurons to visual stimulation and the related columnar organization can be reproduced based on the competition between ON- and OFF-center inputs. Furthermore, the relationships between anatomical neural organization and its physiological response properties are clarified. This model also predicts new columnar organization linking the symmetry of receptive fields, which has never been examined. A hypercolumn, composed of orientation columns and symmetry columns, is suggested to serve as a basis for the representation of visual information.

Roles of visual experience and intrinsic mechanism in the activity-dependent self-organization of orientation maps: theory and experiment

It is widely accepted that functional maps in the mammalian visual cortex such as ocular dominance columns and orientation columns are formed depending on neural activity. There is still, however, controversy on how much visual experience contributes to the map formation during development. In the present study, we address this issue from mathematical modeling and experimental investigation. Using a model of activity-dependent self-organization of geniculo-cortical afferent inputs, we showed that spontaneous activity in the LGN can produce orientation maps, while the exposure to drifting gratings results in sharply segregated orientation maps as observed in cat visual cortex. The restricted exposure to a single orientation of the grating led to the over-representation of the exposed orientation, which was moderated by the contribution of learning based on the spontaneous activity. These theoretical results were confirmed by intrinsic optical recordings from area 18 of kittens reared under various visual conditions.

Cortical direction selectivity without directional experience

HOW neurones in the visual cortex acquire their response properties during postnatal development is an important question with far-reaching implications. In the present study, we demonstrate the developmental specification of geniculo-cortical afferents using our previously proposed model for the activity-dependent self-organization of neural networks. Our results indicate, in contrast to common beliefs, that both orientation and direction selectivity can be achieved in the primary visual cortex even if the retinae were never exposed to oriented and/or moving objects during development.

Identification of ocular dominance domains in New World owl monkeys by immediate-early gene expression

Significance Ocular dominance columns (ODCs), the segregation of activation patterns from each eye in primary visual cortex, are variable in form but are present in most studied primates. However, their existence seems to be weak or absent in nocturnal owl monkeys, raising questions about the significance of ODCs. Using the highly sensitive method of immediate-early genes after monocular deprivation, we revealed an unusual pattern of eye-dependent activity in V1, providing further evidence for the widespread presence and variability of ODCs in primates and raising further questions about their development and functions. Ocular dominance columns (ODCs) have been well studied in the striate cortex (V1) of macaques, as well defined arrays of columnar structure that receive inputs from one eye or the other, whereas ODC expression seems more obscure in some New World primate species. ODCs have been identified by means of eye injections of transneuronal transporters and examination of cytochrome oxidase (CO) activity patterns after monocular enucleation. More recently, live-imaging techniques have been used to reveal ODCs. Here, we used the expression of immediate-early genes (IEGs), protooncogene, c-Fos, and zinc finger protein, Zif268, after monocular inactivation (MI) to identify ODCs in V1 of New World owl monkeys. Because IEG expression is more sensitive to activity changes than CO expression, it is capable of revealing activity maps in all layers throughout V1 and demonstrating brief activity changes within a couple of hours. Using IEGs, we not only revealed apparent ODCs in owl monkeys but also discovered a number of unique features of their ODCs. Distinct from those in macaques, these ODCs sometimes bridged to other columns in layer 4 (Brodmann layer 4C ). CO blobs straddled ODC borders in the central visual field, whereas they centered ODC patches in the peripheral visual field. In one case, the ODC pattern continued into V2. Finally, an elevation of IEG expression in layer 4 (4C) was observed along ODC borders after only brief MI. Our data provide insights into the structure and variability of ODCs in primates and revive debate over the functions and development of ODCs.

Constraint on the number of synaptic inputs to a visual cortical neuron controls receptive field formation

To date, Hebbian learning combined with some form of constraint on synaptic inputs has been demonstrated to describe well the development of neural networks. The previous models revealed mathematically the importance of synaptic constraints to reproduce orientation selectivity in the visual cortical neurons, but biological mechanisms underlying such constraints remain unclear. In this study, we addressed this issue by formulating a synaptic constraint based on activity-dependent mechanisms of synaptic changes. Particularly, considering metabotropic glutamate receptor-mediated long-term depression, we derived synaptic constraint that suppresses the number of inputs from individual presynaptic neurons. We performed computer simulations of the activity-dependent self-organization of geniculocortical inputs with the synaptic constraint and examined the formation of receptive fields (RFs) of model visual cortical neurons. When we changed the magnitude of the synaptic constraint, we found the emergence of distinct RF structures such as concentric RFs, simple-cell-like RFs, and double-oriented RFs and also a gradual transition between spatiotemporal separable and inseparable RFs. Thus, the model based on the synaptic constraint derived from biological consideration can account systematically for the repertoire of RF structures observed in the primary visual cortices of different species for the first time.

Experience-Dependent Self-Organization of Visual Cortical Receptive Fields and Maps

It has been revealed that neurons that selectively respond to similar stimulus features are systematically arranged in the visual cortex to form columnar structures such as ocular dominance, orientation, and direction-of-motion columns [1, 2]. Since Blakemore and Cooper [3] reported that preferred orientations were strongly biased to an experienced orientation for kittens that had stayed inside a cylindrical room and been exposed to a stripe painted on the inner wall of the room, many investigators [3–10] have attempted to elucidate the role of visual experience in the emergence of orientation- and direction-selective cells and related columnar structures. On the other hand, Crair et al. [10] have suggested that visually driven activity is not required for orientation map formation and full maturation of orientation selectivity. It seems to be accepted that the basic structure of orientation maps is unexpectedly robust against restricted visual experience [5, 6, 10].