Normal and anomalous development of visual motion processing: motion coherence and ‘dorsal-stream vulnerability’
Introduction
The detection of motion is one of the most pervasive features of the visual system. In every species where neuroscientists have looked for visual motion sensitivity—from flies (Egelhaaf & Borst, 1993), beetles (Hassenstein & Reichardt, 1956), crabs (Zeil & Zanker, 1997) and frogs (Barlow, 1953), to rabbits (Barlow & Hill, 1963a), cats (Hubel & Wiesel, 1962) and primates (Hubel & Wiesel, 1968)—it has been found. Motion detection is basic to perception, cognition and action. It contributes to a great range of visual functions, including scene segmentation, depth perception, postural and oculomotor stabilisation, recognition of characteristic kinematic events such as the actions of other individuals, and the control of actions in dynamic situations. Moving targets have a high salience in attracting attention in the peripheral visual field. Motion is continually present in the visual image, through eye movements, self-motion, and the motion of external objects. We expect, therefore, that the development of visual motion processing will be a very important part of the overall development of vision in infancy. We might also expect, given the range of processes depending on motion detection, that it would develop early.
To examine this question, we need to have a clear understanding of what constitutes evidence for visual motion processing. Moving stimuli produce local changes in luminance and contrast as they pass over the retina, and so will excite any neurons that are responsive to change. Infants in the first month of postnatal life are sensitive to remarkably high rates of flicker, reflected in a behavioural preference for a large flickering field over a static field of matched mean luminance (Regal, 1981). This general sensitivity to dynamic stimuli can explain the fact that very young infants will orient to a moving target (Volkmann & Dobson, 1976). In terms of contrast detection and acuity, which develop rapidly in the first 3 months of life, motion benefits infants’ sensitivity to low spatial frequency gratings, but only to the same degree as for adults (Atkinson, Braddick, & Moar, 1977). However, infants’ sensitivity and preference for dynamic stimuli do not necessarily imply that the infant’s visual system can extract motion information. The perceptual tasks dependent on motion—depth from optic flow, recognising biological motion, control of dynamic actions—need the visual system to represent the direction and speed of local motion. In visual neurophysiology, the classic criterion that a neuron is concerned with motion processing is directional selectivity—a differential response to the same target moving with equal speed in opposite directions. To state that an infant is processing visual motion, we shall similarly require evidence that the visual system is responding to directional information.
Evidence that a directional system is operating at birth is provided by the eye movements of optokinetic nystagmus (OKN) which follow the direction of large-field movement. The direction of movement must be registered somewhere in the infant’s visual system, but we shall discuss the evidence in 11 The optokinetic response and pursuit eye movements in infancy, 12 Developmental asymmetries of motion processing that this is a reflex, subcortical system that is distinct from the cortical directional systems which provide the basis for motion discrimination and movement-based perceptual skills.
We will discuss cortical motion systems first, going from simple relative motion perception to global processing, and then compare these systems with the subcortical OKN system. Cortical and subcortical systems must operate in a unified way, linking top–down and bottom–up and feeding through to motor control and frontal executive systems. Infants start using cortical systems around 2–3 months of age, but are not tuned as highly as the adult system until much later in life. Adult motion coherence thresholds, for example, are not reached until around 8–10 years of age. We trace this development, reviewing research under a number of subheadings:
- •
Neural systems of motion processing from physiological and anatomical evidence.
- •
Development of directional sensitivity in infants from visual evoked potential (VEP) and behavioural studies, using both uniform and non-uniform motion, and the case of second-order motion.
- •
Development of global motion processing, an indicator of ‘dorsal’ stream development, which may be compared with global form processing.
- •
Infants’ use of motion information in complex perceptual discriminations
- •
Developmental links between the processing of disparity and global motion within the dorsal stream.
- •
The development of the optokinetic response (OKN), monocular asymmetries of OKN as a signature of subcortical processing, and their relationship to cortical asymmetries.
- •
The relative vulnerability of dorsal-stream development in developmental disorders, indicated by comparison of global motion and form sensitivity
- •
Current neurobiological models of the relation between dorsal and ventral-stream development.
Section snippets
Neural systems for motion processing
In primates the retinal and thalamic neurons that form the main pathway to striate cortex are not directionally selective, but directional neurons are common in area V1. The development of motion processing, therefore, is one aspect of the wider development of the selective properties of visual cortex, which begins in human infants in the early postnatal months (Atkinson, 1984, Atkinson, 2000; Braddick, Atkinson, & Wattam-Bell, 1989). Beyond V1, the extrastriate area V5 (also known as MT),
VEP evidence for directional selectivity
Directionally-selective neurons should show a modulation of their responses with a stimulus that periodically reverses its motion between their preferred and non-preferred directions. Directional selectivity in infants can therefore be looked for with scalp recordings of visual evoked potentials that are time-locked to direction reversals. In all tests for directionality, it is important to ensure that temporal integration of the stimulus would not lead to distinctive features in the
Behavioural evidence for directional selectivity
Any developmental argument depends on negative results—a capability which can be demonstrated at age x cannot be demonstrated at some earlier age. The absence of a detectable VEP might arise for a number of reasons and so converging evidence from behavioural techniques is important.
One approach is through preferential looking (PL). In our work, one side of the display contains a uniform pattern of random pixels in oscillatory motion. The other side contains a similar pixel array, but the motion
Uniform and non-uniform motion
A critique of the preferential looking experiments we have described is that they depend on the ability to process direction differences and to use these for segmentation. Plausibly, infants might have an early ability to discriminate local direction in each region, but lack the more complex processing that can derive a visual boundary from the shearing of opposed directions in adjoining regions. No preferential looking test of simple discrimination of a single direction has been devised, but
Second-order motion
Models of directional processing draw a distinction between ‘first-order motion’, carried by luminance variation in the image, and ‘second-order motion’ dependent on the displacement of the pattern of texture, contrast variation, or some other stimulus attribute (Cavanagh and Mather, 1989, Lu and Sperling, 1995). The latter requires a non-linear transformation of the input which according to evidence from psychophysics (Edwards and Badcock, 1995, Ledgeway and Smith, 1993, Lu and Sperling, 1995;
Global motion processing
Studies of motion psychophysics and physiology have distinguished between local motion processing—the sensitivity to direction in a small region of the image, such as a short segment of contour, and global motion processing, which allows the representation of motion over extended regions that may correspond to surfaces and objects (Braddick & Qian, 2000). The latter is usually identified with the integrative properties of V5 neurons, while the former reflects, at least in part, the smaller
Global motion processing compared to global form processing
The development of global motion processing—a function of extrastriate dorsal-stream processing—can be compared with global processing in the ventral-stream domain of form. We have devised a measure analogous to motion coherence thresholds: subjects must detect the organisation of short line segments into concentric circles, with ‘noise’ introduced by randomising the orientation of a proportion of the line segments. Neurons responding to concentric organisation of this kind have been reported
Use of motion information in higher level visual tasks
The introduction to this paper referred to the wide range of complex tasks which depend on motion information. On the one hand, one might expect that the ability to recognise patterns of biological motion, or to derive that 3D structure of an object from the distribution of optic flow, would require many complex processes to develop beyond the elementary detection of directional motion. On the other hand, some would argue that the visual capabilities of infants may be manifested better in the
Motion processing and disparity processing
There is considerable functional overlap between motion processing and stereopsis. In particular, they are both used for image segmentation and depth processing. This functional overlap is paralleled by their physiology; stereo and motion sensitivity are characteristic aspects of dorsal-stream processing. Indeed, physiological data from other species suggest that from V1 upwards, wherever there is directional selectivity, there is likely to be disparity selectivity—often in the same neurons (
The optokinetic response and pursuit eye movements in infancy
Optokinetic nystagmus is a characteristic reflex response to a large field in uniform motion: the eyes follow the movement smoothly (‘slow phase’), flick back in a saccadic-like ‘fast phase’, and repeat this cycle. As discussed in the introduction, it is readily observed in new-borns (Dayton et al., 1964; Kremenitzer, Vaughan, Kurtzberg, & Dowling, 1979) and indicates that some directional visual mechanism must be present at birth. However, the subcortical circuit through the NOT provides a
Monocular asymmetry of OKN
In binocular viewing, OKN can be readily elicited in either direction from birth. However, when OKN stimuli are presented to one eye only in infants under 3 months, there is a marked asymmetry. OKN occurs for stimuli moving in a temporal-to-nasal direction, but is absent or hard to elicit in the opposite nasal-to-temporal direction (Atkinson, 1979; Atkinson and Braddick, 1981a, Atkinson and Braddick, 1981b, Naegele and Held, 1982). This may also be quantified in terms of the finest moving
Cortical–subcortical interactions
From the evidence we have reviewed, development in infancy involves two distinct motion systems, one cortical and one subcortical. The initial asymmetry of OKN appears to be intrinsic to the midbrain nuclei rather than reflecting cortical input, but certainly involves interaction with cortical systems in the course of development.
It seems implausible that the behavioural and VEP asymmetries reviewed above should be independent of the OKN asymmetry, particularly given that disorders of
Global motion and dorsal-stream vulnerability
As we have discussed earlier (7 Global motion processing, 8 Global motion processing compared to global form processing), signal/noise thresholds for coherent motion can be used as an index of dorsal-stream function. In considering development and pathology, we need to identify delays or deficits that are specific to this system, as distinct from general attentional or other factors which may affect performance on a wide range of tasks. In a number of populations, therefore, we have compared
Conclusion: Current neurobiological model of dorsal and ventral-stream development
Fig. 1 summarises our main findings so far on the relative development of form processing and motion processing mechanisms, which can be thought of as functions of the ventral and dorsal cortical streams, respectively.
We have reviewed evidence that the dorsal stream is more vulnerable in development. This comes from children aged 4 years and over, in whom the parsing of the visual array into globally organised forms appears to develop more securely than the equivalent parsing by relative
Acknowledgements
Work described here was supported by Programme Grant G7908507 from the Medical Research Council. We thank our colleagues in the Visual Development Unit, and collaborators elsewhere, whose work has contributed to the results presented.
References (166)
- et al.
Suppression of the optokinetic reflex in human infants: Implications for stable fixation and shifts of attention
Infant Behavior and Development
(1996) - et al.
Visual segmentation of oriented textures by infants
Behavioural Brain Research
(1992) - et al.
Processing of second-order stimuli in the visual cortex
Progress in Brain Research
(2001) - et al.
Infants’ sensitivity to uniform motion
Vision Research
(1996) - et al.
Infants’ sensitivity to statistical distributions of motion direction and speed
Vision Research
(1999) - et al.
Infant direction discrimination thresholds
Vision Research
(2001) - et al.
Bridging cognition, the brain, and molecular genetics: Evidence from Williams syndrome
Trends in Neurosciences
(1999) - et al.
Infant sensitivity to figural coherence in biomechanical motions
Journal of Experimental Child Psychology
(1984) - et al.
Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain
Current Biology
(2000) - et al.
Contrast sensitivity and coherent motion detection measured at photopic luminance levels in dyslexics and controls
Vision Research
(1995)