Josef P. Rauschecker

A neural network for the processing of optic flow from ego-motion in man and higher mammals

Interest in the processing of optic flow has increased recently in both the neurophysiological and the psychophysical communities. We have designed a neural network model of the visual motion pathway in higher mammals that detects the direction of heading from optic flow. The model is a neural implementation of the subspace algorithm introduced by Heeger and Jepson (1990). We have tested the network in simulations that are closely related to psychophysical and neurophysiological experiments and show that our results are consistent with recent data from both fields. The network reproduces some key properties of human ego-motion perception. At the same time, it produces neurons that are selective for different components of ego-motion flow fields, such as expansions and rotations. These properties are reminiscent of a subclass of neurons in cortical area MSTd, the triple-component neurons. We propose that the output of such neurons could be used to generate a computational map of heading directions in or beyond MST.

Auditory localization behaviour in visually deprived cats

The ability to localize sounds in azimuth was tested in five cats that had been binocularly deprived of vision from birth for several months and in three normal age‐matched controls. Brief tone bursts were presented in an eight‐choice apparatus along 360° of the azimuthal plane at constant elevation. Using positive reinforcement techniques, the cats were trained to walk from the centre of the 3 m diameter circular enclosure to the hidden loudspeakers. The distribution of sound localization error from 55 trials per cat at each speaker position was measured, and its standard deviation was used to assess the precision of sound localization. All cats localized tones straight ahead of them most precisely; performance at lateral and rear positions was gradually less precise. When the sound localization ability of normal and binocularly deprived cats was compared across speakers, a significantly enhanced precision was found for binocularly deprived cats overall (P < 0.002; two‐way analysis of variance). An improvement was found at each individual speaker position, but it was greatest at lateral and rear positions. In two sets of control experiments normal cats were retested (i) in the dark with the aid of an infrared camera and (ii) after 3 months of binocular lid suture. Normal cats in the dark did not show any differences in their sound localization behaviour. Late‐deprived cats showed a tendency for better performance, which fell short of statistical significance. Our results in visually deprived cats agree well with some reports on the sound localization ability of blind humans, but disagree with others. Our data provide support for a hypothesis of compensatory plasticity, in which sensory functions get sharpened with the loss of another modality. They seem to rule out the necessity for vision to play a role in the postnatal calibration of auditory space.

Developmental plasticity and memory

The cerebral cortex of young kittens is known to be highly malleable during early postnatal development. However, most studies of developmental plasticity have been conducted in primary visual cortex. It has long been unclear to what extent similar plasticity exists in higher cortical areas. We have now studied developmental plasticity in the anterior ectosylvian (AE) region of the cats parietal association cortex, which receives input from different sensory modalities. One area in this cortical region, which is predominantly visual in normal cats, area AEV, is taken over almost completely by auditory and somatosensory inputs, when cats are binocularly deprived of vision from birth. Furthermore, when single auditory neurons are tested with sound sources in free-field at different locations, they show sharper spatial tuning in visually deprived cats. This compensatory, crossmodal plasticity was explored at the behavioral level by testing visually deprived cats in an auditory localization task, and these cats could indeed localize sound sources more precisely than normal cats. These findings are interpreted as a form of adaptation of the young brain to an altered environment. Similar adaptation is still possible in adult brains by virtue of associative learning and long-term memory. It is argued that the synaptic mechanisms by which associative memories are stored in the cerebral cortex are similar to those in developmental plasticity, only the increment of learning is smaller in adult animals.

Central core control of developmental plasticity in the kitten visual cortex: II. Electrical activation of mesencephalic and diencephalic projections

SummaryFifteen dark-reared, 4- to 5-week-old kittens were stimulated monocularly with patterned light while they were anesthetized and paralyzed. Six of these kittens were exposed to the light stimuli only, in four kittens the light stimuli were paired with electric stimulation of the mesencephalic reticular formation and in five kittens with electric activation of the medial thalamic nuclei. Throughout the conditioning period, the ocular dominance of neurons in the visual cortex was determined from evoked potentials that were elicited either with electric stimulation of the optic nerves or with phase reversing gratings of variable spatial frequencies. In two kittens, ocular dominance changes were assessed after the end of the conditioning period by analyzing single unit receptive fields. Monocular stimulation with patterned light induced a marked shift of ocular dominance toward the stimulated eye, when the light stimulus was paired with electric activation of either the mesencephalic reticular formation or of the medial thalamus. Moreover, a substantial fraction of cells acquired mature receptive fields. No such changes occurred with light or electric stimulation alone. It is concluded that central core projections which modulate cortical excitability gate experience-dependent modifications of connections in the kitten visual cortex.

Auditory compensation of the effects of visual deprivation in the cat's superior colliculus.

SummaryNeurones in the superior colliculus of normal and visually deprived cats were analyzed for their responses to visual, auditory and somatosensory stimuli. The percentage of auditory-responsive cells throughout all layers had increased from 11% to 42% after binocular deprivation. Some auditory responses were found even in superficial layers. The number of somatosensory responses, though not systematically tested, was also higher in the visually deprived animals. Visually responsive units did not significantly decrease in number, thus resulting in an increased proportion of multisensory neurones. The vigour of auditory responses had increased after visual deprivation, while the vigour of visual responses had decreased significantly. In addition to the auditory effects of visual deprivation found, our study confirms previous findings on the visual effects of visual deprivation in the superior colliculus. Since only qualitative changes of visual responses, but no suppression of visual by non-visual activity was found, the neuronal mechanisms responsible for these changes may be different from competition as present in the visual cortex.

Effects of NMDA antagonists on developmental plasticity in kitten visual cortex

The existence of Hebb synapses in the visual cortex of young kittens has long been postulated. A mechanism for the correlation of activity in simultaneously active pre‐ and postsynaptic neurons could be provided by the properties of the N‐methyl‐d‐aspartate (NMDA) receptor and its associated Ca2+ channel, which opens in a transmitter‐ and voltage‐dependent manner. We have studied the effects on cortical plasticity of blocking NMDA receptors in different ways with competitive and non‐competitive NMDA antagonists.

Thalamo-cortical connections and their correlation with receptive field properties in the cat's lateral suprasylvian visual cortex.

SummaryAreas PMLS and PLLS of the cats lateral suprasylvian visual cortex display an interesting global organization of local features in their single unit response properties: direction preference is centrifugally organized and velocity preference increases with eccentricity. In addition it has previously been shown that binocular interactions are strongest around the visual field center. This characterizes the LS areas as apt for the analysis of optic flow fields and for visual processing in various kinds of visuomotor tasks (Rauschecker et al. 1987). In the present study we analysed the types of input to LS from the optic chiasm, the corpus callosum and from two thalamic relay nuclei (lateral posterior and lateral geniculate) that constitute important sources of afferent information to the LS areas. We were interested in learning how the afferent (and efferent) connections between LS and these structures relate to the response properties of LS neurons. Overlap of an RF into the ipsilateral hemifield was virtually always associated with callosal input. Latency differences between responses to electrical stimulation of the optic chiasm and the thalamic sites indicated almost exclusively fast-conducting Y-input to LS. Correlation of response latencies with receptive field properties revealed the following correspondences: A positive correlation was found between LP-latency and RF-size matching the dependence of RF size on laminar origin. The type of correlation found between LP-latency and directional tuning of LS cells suggests that an interaction between thalamic and other inputs may be responsible for direction selectivity in LS. Finally, correlation of LP-latencies with centrifugal direction preference suggests that this specific property is generated by intracortical wiring rather than by thalamic input.

Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex

Summary and ConclusionsIn six dark reared, 4-weak-old kittens visual experience was restricted to contours of a single orientation, horizontal or vertical, using cylindrical lenses. Subsequently, the deoxyglucose method was used to determine whether these artificial raising conditions had affected the development of orientation columns in the visual cortex. After application of the deoxyglucose pulse one hemifield was stimulated with vertical, the other with horizontal contours. Thus, from interhemispheric comparison, changes in columnar systems corresponding to experienced and inexperienced orientations could be determined. The following results were obtained: (1) Irrespective of the restrictions in visual experience, orientation columns develop in areas 17, 18, 19 and in the visual areas of the posterior suprasylvian sulcus. (2) Within area 17, spacing between columns encoding the same orientations is remarkably regular (1 mm), is not influenced by selective experience and shows only slight interindividual variation. (3) In non-striate areas the spacing of columns is less regular and the spatial frequency of the periodicity is lower. (4) The modifiability of this columnar pattern by selective experience is small within the granular layer of striate cortex but substantial in non-granular layers: Within layer IV columns whose preference corresponds to the experienced orientation are wider and more active than those encoding the orthogonal orientation but the columnar grid remains basically unaltered. Outside layer IV the columnar system is maintained only for columns encoding the experienced orientations. The deprived columns by contrast frequently fail to extend into non-granular layers and remain confined to the vicinity of layer IV. (5) These modifications in the columnar arrangement are more pronounced in striate cortex than in non-striate visual areas and, within the former, more conspicuous in the central than in the peripheral representation of the visual field. It is concluded that within layer IV the blue print for the system of orientation columns is determined by genetic instructions: first order cells in layer IV develop orientation selectivity irrespective of experience whereby the preference for a particular orientation is predetermined by the position in the columnar grid. Dependent on experience is, however, the expansion of the columnar system from layer IV into non-granular layers. It is argued that all distortions following selective rearing can be accounted for by competitive interactions between intracortical pathways, the mechanisms being identical to those established for competitive processes in the domain of ocular dominance columns. It is proposed that such experience dependent modifiability of connections between first and second order cells is a necessary prerequisite for the development of orientation selectivity in cells with large and complex receptive fields.

Motion anisotropies and heading detection

In motion-processing areas of the visual cortex in cats and monkeys, an anisotropic distribution of direction selectivities displays a preference for movements away from the fovea. This ‘centrifugal bias’ has been hypothetically linked to the processing of optic flow fields generated during forward locomotion. In this paper, we show that flow fields induced on the retina in many natural situations of locomotion of higher mammals are indeed qualitatively centrifugal in structure, even when biologically plausible eye movements to stabilize gaze on environmental targets are performed. We propose a network model of heading detection that carries an anisotropy similar to the one found in cat and monkey. In simulations, this model reproduces a number of psychophysical results of human heading detection. It suggests that a recently reported human disability to correctly identify the direction of heading from optic flow when a certain type of eye movement is simulated might be linked to the noncentrifugal structure of the resulting retinal flow field and to the neurophysiological anisotropies.

An illusory transformation in a model of optic flow processing

We present results from computer simulations of a biologically plausible model of heading detection in the visual motion pathway of higher mammals. These simulations are closely related to a recently discovered visual illusion in optic flow processing in humans. The model reproduces the results described for humans and suggests a possible explanation, namely that humans interpret the illusory stimuli in terms of egomotion. It provides further indication that the visual system makes use of visual information to cope with eye movement effects in dealing with optic flow.