Jérôme Ribot

Orientation-restricted continuous visual exposure induces marked reorganization of orientation maps in early life

To elucidate the effect of visual experience on the development of orientation maps, we conducted intrinsic signal optical imaging of the visual cortex of kittens that were continuously exposed to a single orientation through cylindrical-lens-fitted goggles under a freely moving condition starting at post-natal week 3. We observed a rapid reorganization of orientation maps, characterized by extensive representation of exposed orientations with reduced responsiveness to unexposed orientations. The over-representation of exposed orientation was marked for 1-2 weeks of goggle rearing. A longer period of goggle rearing, however, decreased the degree of over-representation, which still remained at a remarkable level. Dark rearing episodes daily interleaved between single orientation exposures moderated the over-representation effect. Unit recording from goggle-reared kittens showed preferred orientations consistent with optical imaging. Using c-Fos immunoreactivity mapping, we showed that the number of neurons strongly responding to the exposed orientation was 3 times larger in a goggle-reared cat than the number of neurons responding to the vertical orientation in a normal cat. Taken together, these results suggest that the reorganization of orientation maps was caused by the expansion of domains maximally responding to exposed orientation as well as the strong reduction of responses to unexposed orientations.

A postnatal critical period for orientation plasticity in the cat visual cortex.

Orientation selectivity of primary visual cortical neurons is an important requisite for shape perception. Although numerous studies have been previously devoted to a question of how orientation selectivity is established and elaborated in early life, how the susceptibility of orientation plasticity to visual experience changes in time remains unclear. In the present study, we showed a postnatal sensitive period profile for the modifiability of orientation selectivity in the visual cortex of kittens reared with head-mounted goggles for stable single-orientation exposure. When goggle rearing (GR) started at P16-P30, 2 weeks of GR induced a marked over-representation of the exposed orientation, and 2 more weeks of GR consolidated the altered orientation maps. GR that started later than P50, in turn, induced the under-representation of the exposed orientation. Orientation plasticity in the most sensitive period was markedly suppressed by cortical infusion of NMDAR antagonist. The present study reveals that the plasticity and consolidation of orientation selectivity in an early life are dynamically regulated in an experience-dependent manner.

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.

Online analysis method for intrinsic signal optical imaging

The intrinsic optical imaging technique has been widely applied for the visualization of functional maps in the sensory cortices of mammals. Many current studies refer this mapping in order to focus thereafter on particular features, at some particular locations: a fast and accurate mapping is therefore required. However, even during a successful experiment, the recorded raw data are usually contaminated by some kinds of noise that cannot necessarily be averaged out over the trials. An adequate image data analysis method has to be applied to extract signals closely related neural activities in response to presented stimuli. Thus far two different analysis methods could be adopted: the band-pass filtering and the GIF method [Yokoo T, Knight BW, Sirovich L. An optimization approach to signal extraction from noisy multivariate data. NeuroImage 2001:14;1309-26]. While the latter one is very efficient but requires the whole data in order to maximize the signal to noise ratio, the simple band-pass filtering technically reaches its limits very quickly. Here we propose another filtering method based on the polynomial subtraction of spatially smoothly modulated components. This simple method can visualize well-organized iso-orientation domains of the cat visual cortex with reliability similar to more sophisticated ones while allowing an online visualization of the clean data.

Sound frequency representation in cat auditory cortex

Using the intrinsic signal optical recording technique, we reconstructed the two-dimensional pattern of stimulus-evoked neuronal activities in the auditory cortex of anesthetized and paralyzed cats. The average magnitude of intrinsic signal in response to a pure tone stimulus increased steadily as the sound pressure level increased. A detailed analysis demonstrated that the evoked signals at early frames were scaled by the sound pressure level, which in turn indicated the presence of a minimum level of sound pressure beyond which stimulus-related intrinsic signal can be generated. Intrinsic signals evoked significantly by pure tone stimuli of different frequencies were localized and arranged in an orderly manner in the middle ectosylvian gyrus, which indicates that the primary auditory field (AI) is tonotopically organized. The arrangement of optimal frequencies obtained from optical recordings of the same auditory cortex, which were conducted on different days, was highly reproducible. Furthermore, other auditory fields surrounding AI in the recorded area were allocated based on the observed tonotopicity. We also conducted unit recordings on the cats used for optical recording with the same set of acoustic stimuli. The gross feature of the arrangement of optimal frequencies determined by unit recordings agreed with the tonotopic arrangement determined by the optical recording, although the precise agreement was not obtained.

Preservation of functional architecture in visual cortex of cats with experimentally induced hydrocephalus.

We investigated how neural function is preserved or matured in the visual cortex of cats, following the induction of hydrocephalus by kaolin injection. In vivo optical imaging of intrinsic signals in 11–17‐week‐old hydrocephalic cats revealed orientation maps showing the orderly arrangement of preferred orientations when stimulated by grating stimuli at a low spatial frequency, whereas stimulus‐evoked intrinsic signals in response to gratings at a high spatial frequency were often too weak to construct orientation maps. Furthermore, in two of the three hydrocephalic cats, initially deteriorated orientation maps became almost regular maps in the second imaging experiments conducted 8 and 11 weeks, respectively, after the first imaging. This indicates that, despite large structural deformation of the hydrocephalic brain, orientation maps are elaborated sufficiently after the age of 5–6 months, by which time the orientation map formation is usually completed in normal cats. Single unit recording from the decompressed visual cortex revealed that many neurons showed normal orientation selectivity, whereas the binocularity of these neurons was found to be reduced. These results suggested that the deformed visual cortex of hydrocephalic cats exhibits a high plasticity, retaining its functional organization.

Chronically mountable goggles for persistent exposure to single orientation.

To examine the effect of experience on the developmental plasticity of functional maps in the visual cortex, we need to establish a method for a stable visual experience manipulation under the freely moving condition. For this purpose, we fabricated goggles that are chronically mounted stably on the animals head, but easy to replace according to the animals growth. Here we report the design of the goggles and the method of mounting them on the head of animals. By this method, combined with the intrinsic signal optical imaging technique, we were able to observe a rapid and robust reorganization of orientation maps.

Long-range horizontal connections assist the formation of robust orientation maps

In layer II/III of cat area 17, pyramidal cells and large basket cells are known to form long-range excitatory and inhibitory connections, respectively. The long-range horizontal connections (LRHCs) of pyramidal cells have the tendency to contact other cells with similar orientation preference, in a clustered or anisotropic fashion, up to 8mm away from the cell body [1]. They are believed to be modulatory in nature and permit cortical neurons to integrate information from outside their classical receptive field. Furthermore, electrophysiological studies have illustrated that contextual stimuli mediate both facilitative and suppressive effects, thereby suggesting a functional role [1, 2].

Effects of Chronic Exposure to Vertical Orientation on the Development of Orientation Preference Maps

How the functional maps develop during the critical period of the visual cortex is one of the major questions that have challenged many experimental and theoretical investigators. Although it is accepted that visual experience contributes to the maturation of ocular dominance and orientation maps, how and to what extent visual experience affects map formation has not been fully elucidated yet. Blakemore and Cooper [1] have reported that neurons in area 17 exhibited orientation polar histograms strongly biased to the experienced orientation in cats that had been exposed to only vertical or horizontal stripes in a cylindrical room for several hours a day during development. Although such a strong bias of preferred orientations could not be reproduced by other groups following almost the same experimental protocol [2, 3], many investigators were motivated to investigate the role of visual experience for orientation map formation. Recently, Sengpiel et al. [4] have shown by intrinsic optical recording that the basic structure of orientation maps is rather robust even when the experienced orientation is slightly overrepresented in the visual cortex. It is thought that the discrepancy between the results is partly due to the difficulty in achieving perfect restriction of stimulus orientations for a long time. In this study, we mounted chronically special goggles made of cylindrical lenses on kittens to restrict their exposure to a single orientation during development. Only vertically elongated images of the environment could be seen through the goggles. We recorded intrinsic optical signals from the visual cortex of these kittens, and demonstrated that vertical orientation was strongly overrepresented in all the animals examined. The degree of overrepresentation for the goggles-mounted kittens was much stronger than that for a kitten exposed to vertical stripes inside a cylindrical room.