How Are Visual Areas of the Brain Connected to Motor Areas for the Sensory Guidance of Movement?

R EVIEW How are visual areas of the brain connected to motor areas for the sensory guidance of movement?

Mitchell Glickstein

Visual areas of the brain must be connected to motor areas for the sensory guidance of movement.The first step in the pathway from the primary visual cortex is by way of the dorsal stream of visual areas in the parietal lobe.The fact that monkeys can still guide their limbs visually after cortico–cortical fibres have been severed suggests that there are subcortical routes that link visual and motor areas of the brain.The pathway that runs from the pons and cerebellum is the largest of these. Pontine cells that receive inputs from visual cortical areas or the superior colliculus respond vigorously to appropriate visual stimuli and project widely on the cerebellar cortex. A challenge for future research is to elucidate the role of these cerebellar target areas in visuo–motor control. Trends Neurosci. (2000) 23, 613–617

OST HUMAN and animal movements are Munk4 discovered that unilateral lesions of the stri- Munder continual sensory guidance. In humans ate cortex of the occipital lobe in monkeys produced and the higher primates, the dominant sense that hemianopia, that is, the monkey became blind in controls movement is vision. One of the central the visual field on the opposite side to the lesion. problems in neuroscience is to understand how the Munk’s identification of the visual functions of the brain uses visual input to control whole body move- occipital lobe was confirmed in humans by ments, such as walking through a crowded railroad Henschen5. Henschen identified the cortex on the station without bumping into other people or run- banks, lips and depths of the calcarine fissure as the ning to catch a ball. What are the pathways in the crucial locus of lesions that are associated with brain that are involved in more delicate movements, hemianopia, because damage to cortex outside this such as threading a needle or picking ripe fruit from area failed to produce hemianopia. However, the a vine? When analyzed in detail, what might appear lesions in Henschen’s patients were large and dif- to be a simple directed action might, in fact, consist fuse, which made it difficult for him to establish pre- of several independent components. Jeannerod and cisely how visual fields are represented on the cor- colleagues1, for example, showed that there are at tex. Henschen was correct in identifying the left least two independent mechanisms that control occipital lobe as receiving its input from the left half what appears to be a simple, integrated act of reach- of each retina, hence the right half of the visual ing out to grasp an object. Sakata and colleagues2 field. He also correctly identified the upper bank of have identified an area, the anterior interparietal the calcarine fissures as receiving its input from the area (AIP), within the rostral bank of the intrapari- upper retina, hence the lower visual field. However, etal sulcus, which contains neurones that extract Henschen believed (incorrectly) that the central detailed visual information about the nature of the visual fields were represented anteriorly within the object to be grasped and that is reciprocally con- calcarine fissure. Smaller lesions were required to nected to a motor area within the frontal lobe. determine the precise way in which the visual fields Although the location of the primary visual areas are mapped. Inouye6,7 studied the visual deficits in and motor areas of the cerebral cortex has been brain injured soldiers of the Russo–Japanese war. In known for more than a century and a great deal is many of his patients, a small bullet penetrated the now known about the further processing of the skull at high velocity, leaving a straight track of visual input and the interconnections and projec- injury through the brain. Inouye could therefore use tions of the motor areas3, little is known about how the location of the entrance and exit wounds to cal- these areas are linked. Ultimately, cortical visual culate where the bullet would have crossed the areas must be connected to descending pathways for visual cortex or interrupted the visual radiations. He the control of movement. Although there are inter- studied the visual field defects in these soldiers and Mitchell Glickstein connections between the parietal lobe visual and accordingly constructed a map of how the visual is at the Dept of frontal motor areas, visual and motor cortical areas fields are represented on the striate cortex. The cen- Anatomy, are also strongly linked by way of a pathway tral fields were represented caudally and occupied a University College through the cerebellum. larger cortical area than the peripheral fields. London, Gower The primary sensory and motor areas of the ce- Holmes and Lister8, studied British casualties in Street, London, UK rebral cortex were first identified in the 19th century. the First World War and provided a more detailed WC1E 6BT.

representation of the mapping of the visual fields on Although the current terminology is more sophis- the human striate cortex, which has been repeatedly ticated, the assumption that a series of cortico–cor- confirmed since that time. tical fibres links sensory areas to motor areas of the Identification of the motor area of the cerebral cortex still prevails. There are no direct anatomical cortex also began with animal experiments. Fritsch projections from primary visual cortex (Area 17) to and Hitzig9 showed that weak electrical stimulation the motor and premotor areas (Areas 4 and 6). of a specific region of the dog’s frontal cerebral cor- Instead, cortico–cortical links between the primary tex could elicit movement of the face or limb on the visual and motor areas are indirect and the pathway contralateral side of the body. If electrical stimula- is typically thought to involve a series of tion of a given point elicited limb movement, abla- cortico–cortical links that originate in Area 17 and tion of the cortex at that point hindered the use of end in Areas 4, 6 or 8 for the visual guidance of the that limb. Shortly thereafter, Betz10 described the fingers, limbs or eyes. The corpus callosum is characteristic large pyramidal cells in layer V of cor- thought to mediate tasks in which the visual cortex tex that are associated with the motor area. The on one side had to be linked to the motor cortex on interpretation of these experiments as indicating a the opposite hemisphere. motor-control area in the cerebral cortex was ini- The dorsal stream of extrastriate visual areas tially controversial because some authors insisted that the stimulation must have caused a sensation, In 1982, Ungerleider and Mishkin proposed12 that and it was that sensation which led to movement. the extrastriate visual areas could be broadly segre- Nevertheless, by 1900 the identity and location of gated into two streams on the basis of anatomical the primary sensory and motor cortical areas were and behavioural evidence: one dorsal stream, cod- widely accepted. ing the location of visual objects (‘where is it?’) and Although the evidence for localization of visual and the other ventral stream, identifying the nature of motor functions was clear, surprisingly few questions the object (‘what is it?). In the same year, Jack May were asked regarding how sensory areas might be and I13 proposed that a similar dichotomy exists linked to motor areas for the sensory guidance of between dorsal and ventral extrastriate cortical movement. Most authors assumed that there must be visual areas on the basis of the differential projec- a series of cortico–cortical connections that arise in tions of these two areas to the pontine nuclei. The the visual cortex and end in the motor cortex. Figure 1 dorsal, parietal areas project heavily to the cerebel- reflects this generally accepted view. lum by way of the pontine nuclei, whereas the ventral stream has little or no such projection. We suggested that an important function of the parietal lobe visual areas might be in the visual control of movement, based on its anatomical connections to the cerebellum (Fig. 2). Although visually guided movement of the wrist R a c R and fingers of monkeys is impaired following parietal lobe lesions, control lesions of the temporal lobe or peri-arcuate cortex produce little or no a impairment. The evidence is now clear that the first a step in the pathway that links visual to motor corti- c cal areas is by way of the dorsal stream of extrastriate visual areas, because lesions of these areas in fe fe monkeys profoundly impair visual guidance of movement14. By contrast, lesions of cortical areas in fa fa the ventral stream can impair form, colour or face recognition, but do not affect visuo–motor coordi- nation15. Indeed lesions of the dorsal stream visual areas are so severe in their effects on visual control of movement that Ferrier16,17 initially misinterpreted these effects in monkeys as blindness (Fig. 3). Almost identical deficits in visually guided movement are present in humans after lesions of analogous extrastriate cortical visual areas18,19. Connections of the dorsal stream visual areas k How do the dorsal stream visual areas connect to cortical and subcortical brain areas that control movement? Although there are indirect cortico– trends in Neurosciences cortical routes from these areas to Areas 4 and 6, monkeys can still execute rapid and accurate visually Fig. 1. Cortico–cortical connections between the visual and motor guided arm movements after the white matter cortex after Bernstein. Arrows represent afferent input to (upward, fa) between the parietal lobe visual areas and the frontal and motor output from (downward, fe) the cerebral cortex, respectively. 20 21 Sensory areas are linked to motor areas by a series of cortico–cortical lobe has been cut . Haaxma and Kuypers later fibres, a. The corpus callosum, c, links the two cerebral hemispheres showed that such fibre lesions could produce deficits across the midline. R is an abbreviation for the German Rind or cortex in the visual guidance of wrist and fingers. However, and k indicates the midline. Reproduced from Ref. 11. all but two of the fibre lesions were placed caudally,

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(a) Preop. Bilateral 1.0

0.5

trends in Neurosciences trials on slotted disc slotted on trials Proportion of correct of Proportion 0 p1

3 6 9 3 6 9 12 15 18 21 24 27 30 32 36 Fig. 3. Ferrier’s observation of the visuo–motor deficit produced by a lesion of the parietal lobe visual areas. The deficit was so severe Sessions that Ferrier assumed that the monkey must have been blinded by the lesion. The shaded portions indicate the lesions of the cortex of the (b) hemispheres of monkeys. Top panel shows the right side of the brain Preop. Unilateral Bilateral and the lower panel shows the left side of the brain. Reproduced 1.0 a1 a2 from Ref. 16. a2 that are involved in the control of eye and limb move- 0.5 ments. In addition, Strick et al.3 have studied in detail the interconnections and output of several motor cor-

trials on slotted disc slotted on trials tical areas within the frontal lobes. Far less is known Proportion of correct of Proportion 0 about the links between visual and motor areas of the 3 6 9 3 6 9 12 15 18 21 24 27 30 32 36 cerebral cortex, but it is clear that cortico–cortical Sessions links between the primary visual and motor areas are complex and involve a series of cortico–cortical links. (c) Nevertheless, cortico–cortical circuits cannot account Preop. Bilateral for all examples of sensory-guided movement. 1.0 Therefore, there must be other, subcortical routes whereby sensory information can access motor struc- tures. Two prominent subcortical pathways could, in 0.5 principle, function in the sensory guidance of movement. One possibility would be a pathway via the

basal ganglia. However, although there are visual trials on slotted disc slotted on trials Proportion of correct of Proportion 0 inputs to the caudate nucleus and claustrum23, there is 3 6 9 3 6 9 12 15 18 21 24 27 30 32 36 a much larger route through the pontine nuclei to the Sessions cerebellum24. trends in Neurosciences Pontine nuclei are the major brainstem target of Fig. 2. Performance of monkeys before and after cortical lesions on efferent fibres from the cerebral cortex 21 a visuo– motor task devised by Haaxma and Kuypers . The lesions Nearly all of the descending projections from the are represented in dark grey on the figure. The animals are required to cerebral cortex to the midbrain and below are carried reach out to a disc containing slots at various orientations for a food reward. To perform the task successfully the animal must orient its in the massive Crura cerebri, the large-fibre system at wrist and fingers to conform to the orientation of the slot. The data the base of the cerebral peduncles. A small percentage from five animals are presented. (a) Two monkeys (p1, solid circles and of these fibres travel past the pons and medulla to p2, open circles) had lesions that destroyed most of the dorsal stream become cortico–spinal fibres (Fig. 4). Estimates based of visual processing areas. (b) Two monkeys (a1, solid circles and a2, on light microscopy suggest that there are 20 million open circles) had sequential lesions restricted to the cerebral cortex on fibres in the peduncles and only one million fibres in the rostral bank of the arcuate sulcus and the cortex just rostral to it. the cortico–spinal tracts25. The great majority of The figure shows performance on the disc using the hand contralateral peduncle fibres end in the pontine nuclei. The possi- to the arcuate lesion after the unilateral ablation, and performance bility that cortico–spinal and cortico–bulbar fibres after bilateral lesion by monkey a2. (c) One monkey had a large bilat- also give off collaterals to pontine cells as they pass eral lesion of inferotemporal cortex. The two animals in which the dor- 26,27 sal extrastriate visual areas had been removed were profoundly through the pons , suggests that every fibre in the impaired in guiding the orientation of their wrists and fingers. The cerebral peduncles has a pontine target. Pontine three control animals (b and c) were mildly impaired or unaffected by nuclei, cerebellar hemispheres and lateral cerebellar the lesion. Reproduced, with permission, from Ref. 13. nuclei are especially prominent, in humans and the higher primates28. One of the major circuits through the human brain is a route that originates in the ce- within the parietal lobe visual areas, which would rebral cortex and connects to the cerebellum by way have interrupted descending as well as cortico–corti- of the pontine nuclei. cal fibres. In one of the two cases in which the fibre Dorsal stream visual areas project to the pontine cuts were made more-rostrally, the visuo–motor nuclei deficit was less severe. In the past two decades, there has been an explo- The dorsal stream visual areas are connected to sion of new information about the interconnections the cerebellum by way of a relay in the pontine and response properties of neurones that process nuclei. Degeneration staining and the study of visual information for the control of movement. For orthogradely labelled fibres following a tracer injec- example, Andersen et al.22 described the response tion into the cerebral cortex have revealed a massive properties of neurones in the posterior parietal lobe connection between the dorsal stream visual areas

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(a) (b) (c) paramedian lobule and Crus I and II of the cerebellar hemispheres and to lobule VII of the vermis. Cerebellum projections to nuclei controlling descending motor systems The output of the cerebellar cortex is from Purkinje cells that project to the cerebellar nuclei. trends in Neurosciences The cerebellar nuclei, in turn, Fig. 4. Cross-section through the human brain at different rostro-caudal levels, stained for fibres. (a) Fibre- project directly or indirectly to stained (blue/black) cross-section at the level of the midbrain. Note the massive fibre collection, the basis pedunculi, the cells from which the major at the bottom of the brain (arrow). (b) Fibre-stained cross-section through the pontine nuclei. (c) Fibre-stained sec- descending motor tracts origi- tion through the cerebellum and medulla. The cortico–spinal tracts are visible at the base of the brain as the nate. Here, we emphasize the link medullary pyramids (arrow). Compare the area of the pyramidal fibres at this level with that of the fibres in the basis to the motor cortex, which is pedunculi in (a). mediated by a relay in the ventral thalamus. There are also cere- and the pontine nuclei29. Results of studies using bellar projections to the red nucleus, the superior retrograde tracers are consistent with this observa- colliculus and brainstem areas that give rise to tion. If the pontine nuclei are filled with a retro- the descending reticulo–spinal and vestibulo–spinal grade tracer and labelled cells in the cortex are tracts. mapped, a massive input from the dorsal stream Evidence for a role for the cortico–ponto cerebellar parietal lobe visual areas to the pontine nuclei is vis- pathway in the visual guidance of movement ible. By contrast, there are few or no projections from cortical areas in the ventral stream29. Although Although the effects of lesions of the dorsal stream the exact pattern of termination within the pontine of extrastriate visual areas often resemble the nuclei varies among mammals, in all species that visuo–motor deficits produced by cerebellar lesions, have been studied30–32 there is a rich connection much of the evidence for the role of the between cortical visual areas and the pontine nuclei. cortico–ponto–cerebellar pathway in the visual con- In addition to cortical visual areas, the pons also trol of movement remains indirect. One source of receives an input from the superior colliculus and evidence is the fact that skilled bi-manual coordina- pretectum, which provide additional sources of tion can survive section of the forebrain commis- mossy fibre visual information to the cerebellum33,34. sures. In a study of intermanual transfer43, it was found that although section of the corpus callosum Pontine cells respond to appropriate visual blocked the normally strong transfer of somatosen- targets sory information between the two hands, the motor Cells in the pontine nuclei of cats35,36, and mon- habits of testing two unseen objects showed immedi- keys37,38 that receive their input from cortical visual ate transfer when the second, untrained hand was areas or the superior colliculus39 rapidly respond to tested first. We concluded that there must be a sur- appropriate visual stimuli. The optimal stimuli for viving subcortical pathway linking the two sides of activating pontine visual cells are targets that move the brain. Damage to efferent fibres from the parietal in a preferred direction. The receptive fields of pon- lobe to the pontine nuclei can also produce tine visual cells are relatively insensitive to the orien- visuo–motor deficits. For example, a lesion in the tation of visual targets. The properties of pontine caudal limb of the internal capsule that interrupted receptive fields are consistent with their role in pro- connections from parietal lobe visual areas to the viding a major link in the circuit that controls the pontine nuclei produced symptoms that resembled visual guidance of movement. those caused by parietal lobe or cerebellar damage44. Monkeys in which vision is restricted to one hemi- Pontine nuclei project widely on the cerebellar sphere and in which the forebrain commissures have cortex been cut still use the blinded hemisphere to control If wheat germ agglutinin horseradish peroxidase rapid visually guided use of the limb. Auto- (WGA–HRP) is injected among visually activated radiographic evidence suggests that the link from the cells in the pontine nuclei, the input from the dor- seeing hemisphere to the opposite motor cortex is by sal stream of extrastriate visual areas can be con- way of the cerebellum45. Savaki45 trained monkeys, in firmed by mapping the location of retrogradely which the optic tract and forebrain commissures had labelled cortical cells. The projections of these pon- previously been sectioned, to perform a rapidly exe- tine visual cells can be followed by mapping labelled cuted visuo–motor task, using the arm that was ipsi- axon terminals on the cerebellar cortex. Such stud- lateral to the severed optic tract. She studied the dis- ies have revealed that visual ponto–cerebellar fibres tribution of labelled cortical cells in these animals terminate widely on the caudal cerebellum. The that had been injected before testing with 2-deox- densest target in monkeys40, cats41 and rats42 is the glucose as a cell-activity marker. Although no cor- paraflocculus, although the electrophysiological and tico–cortical visual connections to the contralateral behavioural properties of the dorsal paraflocculus, a motor cortex in these animals remained, the region of cerebellar cortex, have not been explored ‘blinded’ motor cortex proved to be active during extensively. There are also projections to the uvula, performance of the task.

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