Movement

Movement is a core deficit in children with SBM. It is apparent at birth, and infants with SBM have poorer upper and lower limb movement quality than peers and are slower than peers to learn to move their arm to activate a mobile (Fletcher et al., 2004). Children with SBM have deficits in three effectors: upper and lower limbs (Hetherington & Dennis, 1999; Dennis et al., 2002) and eyes (Biglan, 1995). Movement variability is related to the integrity of brain regions such as the cerebellum that control truncal and axial movement (Miall et al., 2001), and the cerebellum and midbrain that control eye movements (Leigh & Zee, 1999). Variability in movement is related to both spinal cord and brain, such that the higher the spinal lesion, the more severe the motor deficit (Lonton, 1977) and the more severe the brain impairments in the posterior fossa and midbrain (Fletcher et al., 2005). The movement deficits in children with SBM are similar to those in adults with lesions in the brain areas controlling movement.

Sensorimotor experience creates and reinforces internal representations in the cerebellum, which are sensory-motor states that predict the consequences of motor plans or control the motor plans needed for a desired sensory outcome (Iacoboni, 2001). Children with SBM are less able than peers to use motor exploration to discover appropriate ways of responding (Berthier et al., 2005) and thereby fail to capitalize on existing representations or to create new ones. Their movement deficits have significant implications for ecological function because they limit environmental search and exploration normally effected by movement, and thereby truncate input into motor control systems that facilitate learning from the environment.

Timing

Timing is a core deficit in children with SBM that is also closely linked with cerebellar abnormalities. Timing deficits are evident over a wide age span, are specific to timing operations, vary with the status of key brain structures, and are similar to those reported in adults with cerebellar lesions.

Throughout childhood and adult life, timing mechanisms are involved in motor control and movement coordination (Mauk et al., 2000; Ivry & Richardson, 2002) and synchrony between sensation and movement is facilitated by short duration timing mechanisms. Compared to typically developing age peers, infants with SBM show less synchronous and more poorly organized upper limb coordination (Fletcher et al., 2004). Children and adolescents with SBM have deficits in short-duration timing (perceiving intervals around a half second) and in motor timing (Dennis et al., 2004). Children with SBM show significantly reduced cerebellar volumes on quantitative MRI studies that are correlated with perceptual and motor timing deficits (Dennis et al., 2004). Deficits in short-duration timing are apparent over the life span in individuals with a variety of cerebellar lesions (Ivry & Keele, 1989; Mostofsky et al., 2000, 2004), so the cerebellar timing system shows little or no age-based change.

The ecological importance of timing deficits is considerable. Temporal information helps generate predictions about the durations of different perceptual events (Ivry & Richardson, 2002) and the sensory consequences of movement (Rao et al., 2001). Early motor development (including aspects of timing) helps to shape cognitive development (Thelen & Smith, 1994), and early deficits in motor synchrony are negatively related to later cognitive search and visual memory abilities in infants with SBM (Landry et al., 2003). Many eye-hand tasks require the constant modulation of motor timing. For example, throwing a ball requires that the opening of the fingers to release the ball must occur within a narrow temporal window with respect to the extension of the arm (Hore et al., 1999). Effective on-line movement coordination is impossible if there is a lack of synchrony between sensation and movement.

Attention Orienting

Attention orienting is a core deficit in children with SBM. Orienting deficits are apparent over different segments of the life span in individuals with SBM, are specific to the salience orienting function of attention, arise from a specific set of brain abnormalities, and are similar to those reported in adults with midbrain and posterior cortex lesions.

The environment includes both perceptually salient and cognitively interesting information. Visual attention is controlled by two partially segregated neural systems, one involved in responding to salience and requiring automatic, stimulus-driven orienting, the other involved in goal-directed responding that is driven by knowledge, expectations, and goals (Corbetta & Shulman, 2002).

Babies find salience in their visual world, orienting to something new but maximizing their exploration of novelty by not exploring the same location repetitively (Richards, 2003). Compared to typically developing peers, infants with SBM show developmental lags in orienting to salient faces: until 24 months of age, they take longer than age peers to shift from a perceptually salient stimulus (a beeping light) to a second, face stimulus (Landry et al., 2003).

Orienting may involve either overt movements of the head, eyes, or body, or covert shifts of attention whereby the head, eyes, or body remain stationary. Covert orienting, which changes attention priorities, may be either automatic, as when we orient to salient information, or effortful, as with voluntary shifts of attention to something interesting (Posner & Cohen, 1984; Posner & Raichle, 1994). School-aged children with SBM orient more slowly to, and take longer to disengage from, what has captured their attention (Dennis et al., 2005a), but do not show deficits in orienting to cognitively interesting stimuli, which are under goal-directed, top-down control.

Inhibition of return, the additional time required to react to a target in a previously attended location is a mechanism for adaptive visual search, and increases the chance that exploration will occur with new objects and in new locations (Posner & Cohen, 1984; Klein, 2000). Compared to controls, children with SBM show attenuated inhibition of return in the vertical plane (Dennis et al., 2005b). The midbrain, including the superior colliculus, is part of a circuit that controls orienting to salience (Rafal & Henik, 1994). Children with SBM and tectal beaking, the characteristic midbrain malformation of SBM, are compromised in their ability to orient in their environment, both overtly with eye movement, and covertly, in the manner in which they shift attention. These children show difficulties with orienting to salience and a more attenuated inhibition of return in the vertical plane (Dennis et al., 2005a, 2005b). The principled relations between brain dysmorphologies and posterior attention functions such as covert orienting and inhibition of return can be identified not only in adults, but also in children with congenital malformations of the midbrain and posterior cortex. The posterior attention system shows no obvious age-based differences.

Core deficits in attention orienting have ecological significance throughout the life span. Visual foraging in infants has adaptive significance because it provides detailed information about the external world integrated with spontaneous body movement and goal-directed action during a period when the brain is developing rapidly (Robertson et al., 2001). Exploration of the visual environment regulates opportunities for perceptual-cognitive activity (Robertson et al., 2004), but infants and children with SBM explore space inefficiently.

Primary CNS Insults Cause Core Deficits

Primary CNS insults cause core deficits (Path 2, Figure 1), the evidence being, first, that each core deficit has been clearly related to one or more of the primary CNS insults and, second, that core deficits vary in the degree of expression according to primary CNS insults (the most obvious example being that, compared to those with lower lesions, children with upper spinal cord lesions have more widespread movement limitations). There is no evidence that the magnitude of core deficits is significantly moderated by secondary CNS insults; for example, timing and attention-orienting deficits are related to measures of primary CNS insult, but not to markers of secondary CNS insult, such as number of shunt revisions to control hydrocephalus.

Core deficits are relatively independent. Motor timing in infancy is not related to attention orienting and shows only small to moderate correlations with movement (Fletcher et al., 2004). Other core deficits, such as covert orienting, are apparent when eye movements are restricted (Dennis et al., 2005a), and occur in children with and without major motor deficits (Dennis et al., 2005b). Studies of short duration timing illustrate the independence of timing and movement. Motor tapping deficits in children with SBM are related to the timing or clock component, concerned with the accuracy of the duration between taps, but not to the performance or motor component, concerned with the initiation and termination of the tapping action (Dennis et al., 2004). Furthermore, perceptual timing deficits occur in children with SBM regardless of their motor status (Dennis et al., 2004). Finally, timing deficits and attention-orienting deficits have different neurological bases (Dennis et al., 2004, 2005a, 2005b).

For typically developing individuals, core processes operate together to enhance ecological coherence, so that the individual is attuned to the environment. For many skills, the synchrony of core processes is important. Motor control, for instance, is a product of movement and timing by which movement is temporally synchronized with external stimuli. However, at both a behavioral and a neural level, core deficits are distinct. In individuals with SBM, deficits in one core process need not entail deficits in another, and, furthermore, intact function in one may be associated with deficits in another.

Motor Function: Intact Adaptation (Associative Processing) and Impaired On-Line Control (Assembled Processing)

Despite core deficits in movement, children with SBM exhibit a pattern of intact and impaired motor skills that, as Yeates et al. (in press) have suggested, may be decomposed in accordance with the neuroscience of motor skills. Although deficits in upper and lower extremity motor functions (Grimm, 1976; Hetherington & Dennis, 1999) have long been documented, motor assets have only recently been identified.

Motor adaptation is a change in the control of movements that occurs as a result of repeated task exposure or practice not dependent on conscious recall of the earlier exposure. Motor adaptation is a form of implicit learning, or learning without the intention to learn. New findings showing intact motor learning and motor adaptation in both hand and eye suggests that implicit motor learning (associative processing) may be an asset for children with SBM. They perform similarly to age peers on two measures of motor adaptation: biasing in weight judgments after exposure to heavy versus light weight, adaptation in reaching movement after vision is laterally displaced by prisms (Colvin et al., 2003), as well as procedural motor learning (Edelstein et al., 2004). Adaptive motor learning in children with SBM is intact for eye as well as for limb movement. Children with SBM and controls are equally proficient at making saccadic eye movements under controlled environments, and at modifying saccadic programming by adapting to “jumps” in visual targets below the threshold of conscious awareness (Salman et al., 2005a, 2005b).

In contrast to adaptive motor learning, regulated on-line motor performance of limbs and eyes (assembled processing) is impaired in children with SBM. The same children with SBM who showed procedural motor learning nonetheless had lower initial and final motor performance (Edelstein et al., 2004). Smooth pursuit eye movements are slow and conjugate eye movements that stabilize the image of a moving target on the fovea for high definition vision (Sharpe, 1998). Salman et al. (2005c) found that SBM children with nystagmus (who could adapt to jumps in visual targets) have impaired smooth pursuit movements.

The midline cerebellum calibrates reflex movement of the eyes, whereas the cerebellar hemispheres are concerned with voluntary control of eye movements, including visual fixation, ocular alignment, and smooth pursuit movements (Sharpe, 1998). That children with SBM seem to have particular difficulty with motor functions of the cerebellar hemispheres is consistent with significant reduction in their cerebellar hemispheric volumes (Fletcher et al., 2005).

The neural network of the SBM motor profile is not fully understood. In adults, motor adaptation is related to a neural circuit that involves both the cerebellum and the striatum. In children with SBM, adaptive motor learning is unrelated to measures of cerebellar volume (Edelstein et al., 2004). On-line motor control, which is a function of the posterior parietal cortex in the mature brain (e.g., Pisella et al., 2000), is uncorrelated with structural size of the midsagittal areas of the cerebellar vermis in children with SBM (Salman et al., in press; 2005c). In the adult, automatic and voluntary motor control cortical networks show substantial overlap (e.g., there is an overlapping cortical network for saccades and smooth pursuit movements, Berman et al., 1999), but it is not known whether overlap exists in children with SBM.

Perception: Intact Categorical Perception (Associative Processing) and Impaired Coordinate Perception (Assembled Processing)

Although visual perception was traditionally identified as a problem area in children with SBM, recent research has shown that children with SBM (and other neurodevelopmental disorders, e.g. Williams Syndrome; Bellugi et al., 1994) have relative strengths on visual perception tasks involving categorical relations (e.g., face perception, object perception) and relative deficits on visual perception tasks of figure–ground delineation and relational coordinates (e.g., overlapping objects) (Dennis et al., 2002). Children with SBM have difficulty with coordinate or relational perceptual representations (assembled processing). This is a significant impairment because flexible representations of space guide behaviors as diverse as handwriting, establishing figural contours, and throwing a ball to a target. Perceptual difficulties have been correlated with posterior cortex thinning (Dennis et al., 1981; Fletcher et al., 1996).

Impaired movement is not responsible for the impairment on coordinate perception tasks because children with SBM have difficulties not only on drawing tasks that require both visual perception and motor control, but also on tasks with limited motor components (Fletcher et al., 1992). The distinction between categorical perception and flexible perceptual representations has also been demonstrated among classes of illusory stimuli. Children with SBM can perceive illusory object properties (size, length, contour) but not multistable objects, which require perceptual flexibility and the maintenance of multiple fleeting relations, for instance, between figure and ground (Dennis et al., 2001).

Intact associative processing and impaired assembled processing in visual perception may also be demonstrated in auditory perception. In the domain of music, children with SBM show intact ability to extract pitch feature information on a psychophysical task requiring them to judge variations around a target frequency of 300 Hz (Dennis et al., 2004), but are impaired in assembling temporal information into higher-order rhythmic structures (Hopyan et al., 2003), especially if they have reduced cerebellar volumes (Dennis et al., 2005c).

Memory: Intact Implicit Memory (Associative Processing) and Impaired Explicit Memory (Assembled Processing)

An important theoretical distinction in memory research is that between implicit memory, the learning or facilitation of performance by exposure without intention to remember (associative processing), and explicit memory, the conscious effort to recognize or recall (assembled processing). Children with SBM have relatively intact implicit memory. Using both a perceptual priming task (recognition of fragmented pictures, some of which had been passively encountered earlier) and a conceptual priming task (semantic decisions about words), Yeates and Enrile (2005) found that children with SBM had intact perceptual and semantic priming. In contrast, children with SBM are impaired on explicit memory tests involving different types of content (single word, story, list, design and spatial material) and different indices of memory (cued recall, encoding, recognition, and retrieval) (Yeates et al., 1995; Scott et al., 1998; but see Donders et al., 1991). Memory problems may be the cause of deficits in other domains (e.g., poor working memory is correlated with math problems, Dennis & Barnes, 2002) and/or the results of other domain problems (e.g., memory for designs measured by drawing is likely to be related to spatial and motor problems). Adults with SBM have quite widespread memory problems (Dennis et al., 2000), although the origin of these deficits is not well understood. The neural correlates of memory difficulties in SBM have not been studied.

Language: Intact Grammar and Stipulated Meaning (Associative Processing) and Impaired Constructed Meaning (Assembled Processing)

Although language was once viewed as an asset for children with SBM, recent psycholinguistic and experimental studies of language have suggested a profile of intact and impaired language skills. Children with SBM develop content and function words, and demonstrate facility with grammar and vocabulary, while showing semantic–pragmatic, discourse-level difficulties (Dennis et al., 1994; Barnes & Dennis, 1998). Their strengths are in the formal, fixed structures of grammar, and single words or phrases and meanings that represent stored associations; their weaknesses are in assembling on-line meaning by integrating words, world knowledge, and context.

Meaning may involve the passive activation of frozen meaning or stipulated information, such as is involved in dictionary entries of lexical items. Meaning is also an active process that involves on-line assembly, suppression, and integration of information from the current oral or written text, real-world knowledge, and a representation of the situation the text or conversation describes. Preschoolers with SBM produce fewer story elements than age peers (Fletcher et al., 2004). Children with SBM learn, remember, and activate old knowledge better than they assemble meaning using old and new knowledge (e.g., Dennis et al., 1994; Barnes & Dennis, 1998). Children with hydrocephalus, most with SBM, continue to show particular difficulty with the assembly, suppression, and integration components of language (Barnes et al., 2004). Deficient suppression may preempt other comprehension processing resources and provide incomplete input to mental computations that generate a well-specified semantic representation (Tompkins et al., 2001). In accordance with this, children with SBM have poorly specified semantic representations that contain extraneous, contextually irrelevant information, which might explain why their conversations are referentially underspecified and tangential.

Idiom comprehension provides a clear example of the distinction between intact associative and impaired assembled meaning in children with SBM (Huber-Okrainec et al., 2005). Children with SBM can understand frozen idioms that are processed as a lexicalized unit, but have difficulty understanding novel idioms constructed from context. Specifically, they show a comprehension advantage for decomposable idioms whose meaning can be directly accessed by regular nonfigurative language mechanisms (e.g., a mile a minute) over nondecomposable idioms whose meaning needs to be constructed using context (e.g., kick the bucket) (Huber-Okrainec et al., 2005). Within the domain of figurative language, performance varies with the demands of assembled processing. Huber-Okrainec et al. (2005) report more severe idiom comprehension deficits in children with SBM who had more severe callosal abnormalities.

Reading: Intact Word Recognition (Associative Processing) and Impaired Reading Comprehension (Assembled Processing)

Reading decoding requires the activation of previously formed associations, in contrast to reading comprehension, in which world knowledge is combined with text to construct meaning and text representations. Reading comprehension, but not reading decoding, is related to general cognitive ability (Shatil & Share, 2003).

Children with SBM can decode words better than they can understand texts. Reading comprehension is poorer in children with SBM than in controls (Barnes & Dennis, 1992), even when reading decoding is precisely matched (Barnes et al., 2001). With increasing age, the reading profile stays relatively constant in individuals with SBM (Wills et al., 1990), although limitations in broader aspects of literacy such as writing ability continue into adult life (Barnes & Dennis, 2004).

Math: Intact Calculation (Associative Processing) and Impaired Estimation (Assembled Processing)

Math calculation (associative processing) involves the retrieval of number facts and calculation procedures from memory. Numerical estimation (assembled processing), in contrast, requires that information be accessed and compared with reference to a more abstract rather than exact representation of quantity or extent, and real world estimation requires the integration of quantitative knowledge with knowledge about approximate quantities and sizes of objects. Children with SBM are more accurate on measures of multiplication (presumed to rely on math fact retrieval from semantic memory) than on estimation of size, length, mass, and price, which rely on integration of multiple sources of information (Barnes et al., 2002). Within exact calculation, math fact retrieval is more accurate than is the application of procedures or algorithms such as carrying and borrowing (Ayr et al., 2005; Barnes et al., 2005). Within single digit arithmetic, children with SBM and specific math disability are relatively fast at retrieving small number facts (sums < 10), but are slow in solving larger sum problems (sums between 11 and 18). Because large sum facts are less reliably retrieved from semantic memory than small sum facts, these findings suggest that the distinction between associative and assembled processing is found not only between tasks, but also within tasks in which individual items may draw on different types of processing (Barnes et al., 2006). The neural correlates of mathematics have not been explored in SBM.

Behavior: Intact Activation (Associative Processing) and Impaired Regulation (Assembled Processing)

Children with SBM are sociable and appear to activate a range of social behaviors, although they have difficulty in behavior regulation. Preschool children with SBM require more hints from a familiar examiner about how to involve a naïve examiner in a social party (Fletcher et al., 2004). In preschoolers, difficulties with behavior regulation are related to an inability to apply rules discovered through instruction and social interaction (Landry, 2005). School-aged children with SBM have a range of difficulties, including problems identifying the rules underlying effective goal-directed behavior in social situations, and maintaining goal-directed activities during play (Landry et al., 1993b); difficulties in unstructured social situations, showing inappropriate social distance, hyperverbosity, inappropriate use of language, tangential speech, and a failure to benefit from feedback or instruction about their behavior (Barnes & Dennis, 1998); and difficulty with social problem solving, including production of contextually appropriate responses to social interactions and comprehension of the social expression of emotion (Landry et al., 1993a; Koval, 2004). Neural correlates of behavioral difficulties have not been identified.

Secondary CNS Insults

Secondary CNS insults (Box, Figure 1) moderate assembled processing (Path 5, Figure 1). The effect of secondary insults begins before birth, and may continue throughout life. A thin posterior cortex is associated with more impairment in visual perception and visuo-motor function (Dennis et al., 1981; Fletcher et al., 1996). Young adults with SBM exhibit math deficits, the magnitude of which varies with lifetime shunt revision history (Dennis & Barnes, 2002). The magnitude of some language comprehension deficits in children with SBM is related to corpus callosum hypoplasia (thinning secondary to hydrocephalus), as well as congenital dysgenesis (Huber-Okrainec et al., 2005). Interhemispheric communication as assessed by dichotic listening tests, on the other hand, is related to the presence of splenial dysgenesis and not to corpus callosum thinning (Hannay et al., 2004). Secondary CNS insults appear to have fewer moderating effects on associative processing.

Environment

Core deficits exert an influence on the environment of the child with SBM (Path 6, Figure 1), so that environmental challenges are greater for children with more severe core deficits. Children with upper spinal lesions, for example, have more significant limitations on mobility, orthopedic and urologic function (Lonton, 1977), and require more economic and care-giving resources than do children with less impaired movement.

Environmental factors such as poverty, parental education, care giving, and parenting constitute a second set of moderators that begin before birth and continue throughout life. Poverty lowers general ability in children with SBM, especially in language (Fletcher et al., 2005), and disadvantaged children with SBM have lower Verbal IQ (Fletcher et al., 2004). Low socioeconomic status contributes to poor social competence (Greenley et al., 2006; Landry et al., 1994). Cognitive and social development is facilitated by parenting that promotes autonomy and independence (Weiss et al., 1992), and cognitive and language development is accelerated in children who receive flexible and responsive parenting (Landry et al., 1997), including children with SBM (Landry, 2005). Family and care-giving factors moderate the effect of SBM on adjustment (Greenley et al., 2006). Socioeconomic status and the presence or absence of family support is likely to influence the provision of appropriate remediation for specific cognitive and academic skills, such as math. Less is understood about how variations in education moderate the cognitive phenotype. For example, children with SBM rarely meet criteria for dyslexia because they can decode words, but the effect of reading comprehension programs have not been evaluated because children with SBM are rarely enrolled in evaluation studies.

Environmental factors (Box, Figure 1) moderate associative processing (Path 7, Figure 1), which, in turn, mediates the status of functional assets (Path 8, Figure 1). Environmental moderators are important, not because of their influence on assembled processing, but because they reduce SBM assets in associative processing, which serves to elevate the overall level of functional disability.