Attentional gating in primary visual cortex: A ...

Perception, 2005, volume 34, pages 903 ^ 911

DOI:10.1068/p5332

Attentional gating in primary visual cortex: A physiological basis for dyslexia Trichur R Vidyasagar

Department of Optometry and Vision Sciences, University of Melbourne, Corner Keppel and Cardigan Streets, Carlton, VIC 3053, Australia; e-mail: [email protected] Received 27 July 2003, in revised form 30 June 2004

Abstract. The visual magnocellular pathway is known to play a central part in visuospatial attention and in directing attention to specific parts of the visual world in serial search. It is proposed that, in the case of reading, this mechanism is trained to perform a sequential gating of visual information coming into the primary visual cortex to enable further orderly processing by the ventral stream. This scheme, taken together with the potential for plasticity between the different afferent channels in the case of a relative impairment of the magnocellular system, can provide some limited rationale for the beneficial effects that have been claimed for the use of coloured overlays and glasses.

1 Introduction It is now well known that there are extensive feedback inputs to early stages of the visual pathway (eg to the striate cortex) that modulate the incoming sensory information (see Salin and Bullier 1995 for review). The feedback inputs that the primary visual cortex (striate cortex, V1) receives from various extrastriate areas may be related to figure ^ ground interactions, contour integration, attention, or even memory (Motter 1993; Lamme 1995; Zipser et al 1996; Vidyasagar 1998, 2001; Ito and Gilbert 1999). In this article I review some of the recent work on attention-related feedback to the striate cortex and, on the basis of these physiological principles, propose how these feedback interactions might be critical in the process of reading, what sort of neural impairments might underlie dyslexia, and also what remedial measures could be supported by this new neurological insight. 2 The magnocellular pathway in attentional selection The three parallel pathways, magnocellular (M), parvocellular (P), and koniocellular (K), that carry inputs from the dorsal lateral geniculate nucleus (LGN) to the primary visual cortex in the primate (Callaway 1998; Hendry and Reid 2000), remain segregated till they arrive at the striate cortex, and also show a fair degree of segregation in and beyond V1 (eg Livingstone and Hubel 1988; Merigan and Maunsell 1993), but there are a number of ways in which this segregation is watered down from V1 onwards (see later). In their further projections, there is also some degree of overlap between the P and M channels (eg Maunsell et al 1990; Merigan and Maunsell 1993; Ferrera et al 1992, 1994). The studies can be summarised by saying that, while the dorsal stream into V5/MT and the posterior parietal cortex is dominated by the M inputs, the ventral stream into the temporal neocortex receives most of the P input and also a not insignificant amount of the M input. As will be described later, there is also some mixing of inputs even at the level of the striate cortex. The general consensus that the ventral stream deals with object recognition and the dorsal stream is more concerned with spatial aspects, such as spatial location, stereopsis, and motion, and that the different stimulus attributes are localised in different cortical areas (eg Livingstone and Hubel 1988; Merigan and Maunsell 1993) throws up a conundrum. How are the different attributes of an object bound together while they

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are being processed by cells in different areas having large receptive fields (Boussaoud et al 1991) with poor location information? A recent model of dyslexia (Vidyasagar 1999) builds upon the `feature integration theory' that seeks to address the binding problem (Treisman and Gelade 1980; Treisman 1988). This theory proposes that an attentional spotlight acting from a master map of locations selects regions of interest at an early stage in the visual pathway. This idea has been elaborated at a neural level (Vidyasagar 1999, 2001) to suggest that the spotlight arises from a dorsal stream structure (probably the posterior parietal cortex) and acts on the primary visual cortex to specifically gate the information entering the ventral stream. There is now robust physiological evidence for attentional modulation of primary visual cortex from both single-neuron (Motter 1993; Vidyasagar 1998) and human imaging (Brefczynski and DeYoe 1999; Gandhi et al 1999; Martinez et al 1999, 2001; Somers et al 1999) studies. These studies generally show that attended locations exhibit increased neuronal responses to visual stimuli and unattended locations reduced responses. Recent psychophysical studies show that serial visual search critically depends upon the M pathway (Cheng et al 2004), suggesting that the attentional spotlight is mediated by an M-dominated feedback from the dorsal stream that gates the P inputs to the ventral stream. The visual latencies seen for MT cells can be as low as 30 ^ 40 ms (Bair et al 2002) and are about 45 ms in the lateral intraparietal area (LIP) of the parietal cortex (Bisley et al 2004), and so the M-dominated feedback to V1 could indeed gate P inputs, which have a mean latency of 87.4 ms in V1 (Nowak et al 1995). It is also worth noting that, in a recent study, Morand et al (2000) have reported a rapid K input reaching the dorsal stream at around the same time as the M input. They identified an early electrical field (with a latency of 40 ^ 75 ms) for tritan motion stimuli in human MT/V5 area, sharing the same neural sites as luminance-induced motion. Consistent with this, we have also seen that visual search with S-cone isolating, blue ^ yellow stimuli is significantly faster than with red ^ green stimuli (Cheng et al, in preparation). 3 Visuospatial attention in reading and dyslexia It has long been suspected that the basic lesion in dyslexia may be a M impairment in the visual pathway (eg Lovegrove et al 1980, 1986, 1990; Livingstone et al 1991; Cornelissen et al 1995, 1998; Borsting et al 1996; Eden et al 1996; Stein and Walsh 1997; Demb et al 1998). At first glance, this may appear odd, since reading would be expected to depend on the fine-pattern vision that the P system is capable of (Kaplan et al 1990) owing to the smaller receptive fields of the P cells and their higher sampling density in the retina. Earlier accounts of the aetiology were directed at a possible role that the M inputs may have in eye movements (Pavlidis 1981) or in keeping the packet of information processed by the P system during each fixation separate from the next packet by a saccade-driven transient (possibly, M-cell) inhibition on sustained (possibly, P-cell) channels (Breitmeyer 1980). However, both these ideas can now be discounted in the face of a number of experiments (Rayner 1985; Morris et al 1990; Burr et al 1994; Vidyasagar 1999). For a detailed account of these arguments see Vidyasagar (1999, 2001, 2004). A recent explanation for how an M deficit could lead to a reading disability depends upon the role that the M system plays in directing focal attention (Vidyasagar 1999; Vidyasagar and Pammer 1999; Facoetti et al 2000; Schulte-Koerne et al 2004). Reading involves periods of fixation punctuated by regular saccades. In languages with left to right scanning, fixations lasting about 250 ms are separated by rightward saccades, with about 7 or 8 letters being read during each fixation period. It has been argued (Vidyasagar 1999) that sequential scanning of the individual letters during the fixation periods is necessary for effective letter identification. Since the large receptive

Parallel pathways and dyslexia

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fields of the ventral stream areas involved in object recognition do not code well for location, feedback from the dorsal stream could feed the letters of each word in a temporal sequence to the ventral stream. This is consistent with the finding that we do not recognise words as wholes, but each letter is individually identified and then strung together (Pelli et al 2003). This neural scheme of reading also explains why learning to read is a difficult process, taking many years. Quite apart from the semantics, the very mechanics of reading are arduous for children to master. The reason for this may be that the normal visual-search process is random and anarchic (Horowitz and Wolfe 1998), with no memory kept for the locations already searched. In the case of reading, this attentional gating has to be trained to go sequentially across the lines of the text. Difficulties in this process can happen even with small lesions affecting the M cells in the critical parts of the visual field, say just to the right of the projection of the centre of the fovea, preventing effective attentional spotlighting over the letters during each fixation. Such small lesions may not always be detectable with the usual tests done to evaluate M function and may explain why some investigators (eg Skottun 2000; Amitay et al 2002) do not agree that there is a specific M impairment. In fact, using a perimetry that seems to detect focal M losses well (Maddess et al 1999; Johnson 2002), Pammer and Wheatley (2001) found that dyslexics have reduced M cell sampling density. This model of dyslexia as a disorder of visuospatial attention is supported by a number of recent studies in which impaired serial visual search (Casco and Prunetti 1996; Vidyasagar and Pammer 1999) and spatial attention deficits (Steinman et al 1998; Facoetti et al 2000) in dyslexics have been reported. 4 Possible neural re-organisation in dyslexia: Is there a rationale for the use of coloured filters? Re-routing of fibres to a target other than the usual one is a manifestation of the plastic potential that many neurons have. The classic example is the ocular dominance shift seen after neonatal monocular lid suture (Wiesel and Hubel 1965; LeVay et al 1980). During early development, geniculate afferents to primary sensory areas compete for the targets in an overlapping cortical zone, but, in the adult, the plasticity is largely restricted to intracortical connections, where the plasticity may be due to functional unmasking of existing connections or due to actual sprouting of nerve terminals (Darian-Smith and Gilbert 1994; Das and Gilbert 1995). This plastic potential, in some cases of developmental lesions, injury or experimental manipulations, can be quite inappropriate. After a cortical area loses its afferent inputs in the adult animal, say after severing of the dorsal roots (Pons et al 1991), amputation of a hand (Ramachandran 1993), or a localised retinal lesion (eg Gilbert 1998; Dreher et al 2001), the de-afferented cortical target now responds to stimuli applied to the sensory surface whose cortical representation is adjacent to the de-afferented site. With this background, let us consider what might be the consequences of loss of inputs to the M targets in the striate cortex, say due to some congenital, developmental or other disease process affecting the geniculo-cortical or retinal M neurons/fibres, or even a non-specific affliction, but one which has a predilection for the larger cells/ fibres. It has indeed been shown that dyslexia is linked to a defect on chromosome 6 (Grigorenko et al 1997; Kaplan et al 2002) at a site possibly related to the development of M cells (Corriveau et al 1998). If the putative lesion in a dyslexic is one that is restricted largely to M cells as claimed by many studies (see above), there are a number of levels where cells which would normally receive M inputs could now receive K or P inputs: (1) The mid-region of striate cortical layer 4C exhibits in normal monkeys an overlap between the M afferents innervating 4Ca above and P afferents innervating 4Cb below, shown anatomically (Yoshioka et al 1994; Levitt et al 1996)

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and physiologically (Vidyasagar et al 2002). (2) Layer 4A receives direct blue/yellow LGN afferents, possibly all belonging to the K pathway (Chatterjee and Callaway 2003). The adjacent layer 4B has long been established as a primary target of M inputs from layer 4Ca (eg Livingstone and Hubel 1988). (3) Supragranular layers of striate cortex receive P, M, and K inputs in its vertically alternating patch (also known as `blob') and interpatch (or interblob) regions, with P and M inputs from layer 4 going mainly to interpatch areas, and K inputs from the LGN to the patch areas (Yoshioka et al 1994; Levitt et al 1996; Callaway 1998). (4) Area V5/MT receives both M and K inputs (Morand et al 2000). Any one or more of the above four sites could be a potential place for plasticity. However, considering that there is so far little evidence for plastic changes occurring across laminar boundaries and most instances of plasticity are across the horizontal extent of the cortex, between columnar modules either in layer 4 (eg LeVay et al 1980) or through lateral interactions in supragranular layers (Gilbert 1998), it is less likely that the M target sites in layer 4 that are poorly driven would be invaded by P afferents. The lateral connections in the supragranular layers seem to be able to mediate plasticity in both the newborn (Dreher et al 2001; Trachtenberg and Stryker 2001) and the adult (Das and Gilbert 1995; Calford et al 2003; Waleszczyk et al 2003). The more likely site of plasticity is a K horizontal invasion of M targets in the supragranular layers of V1. It has been shown recently that the V1 interpatches provide inputs to both pale and thick stripes of V2 (Sincich and Horton 2002b), and the thick stripes of V2 are known to project to V5/MT (Shipp and Zeki 1985; DeYoe et al 1994). This would mean that the thick stripes, which normally send a relatively pure M input to the dorsal stream via its projection to V5/MT can be contaminated by K inputs. There could, additionally, also be an invasion of M targets in area V5/MT from the direct K input (Morand et al 2000) as well as into layer 4B from layer 4A. What would be the perceptual consequence of such a reorganisation? K cells are very likely to carry the blue ON signal from shortwave-sensitive (S) cones in the old world primates (Hendry and Reid 2000) as in the new world primate (Martin et al 1997). However, given the rather poor sampling by S-cones compared to the M and L cones (Roorda and Williams 1999), any contamination of M-cell targets by K inputs via lateral connections in V1 or V5/MT would degrade the spatial signal carried by the M pathway to the dorsal stream and can affect its putative spotlighting function in reading. If the contamination were to arise also from the slower S-cone K inputs (such as the long latency, 175 ^ 240 ms field in V5/MT identified by Morand et al 2000) and possibly from other non-S-cone K inputs, the highly precise spatiotemporal parsing of individual letters needed at the level of V1 could be further compromised. One way of improving the situation may be to use a yellow filter or overlay that would reduce the blue input. The use of coloured filters in dyslexia has had a controversial history since Irlen (1991) first proposed it, partly because the treatment was without any plausible physiological basis. Some (eg Bouldoukian et al 2002; Wilkins 2002), reported beneficial effects from using coloured overlays, but mostly on subjective tests and others have failed to observe any specific improvement in reading (Evans and Drasdo 1991; Menacker et al 1993; Evans et al 1994; Northway 2003). It has, however, been claimed that appropriate choice of colour for the overlay by the subject was essential for improving reading speed (Wilkins 2002). More importantly, a recent randomised double-blind controlled study employing a battery of tests to assess reading ability and a number of other visual functions by Stein's group at the University of Oxford (Stein 2003; Ray et al 2004 and forthcoming), has shown that dyslexic children do improve significantly in reading scores when using a yellow or blue filter of their own choice. The dyslexic children were classified as yellowchoosers and blue-choosers and the children who chose yellow glasses (termed `negative blue'), who actually formed the majority in the Oxford sample, will fit the scenario we have described earlier, where the yellow filter should reduce the interfering blue input.


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Some reading-impaired children seem to benefit from blue, rather than yellow, filters (Wilkins 2002; Stein 2003). This does not fit easily with the above scenario, but it may be the result of a more drastic impairment, which is not restricted to M cells, but also affects the K pathway. The blue-sensitive system appears to be more susceptible to ischaemic and hypoxic insults (eg Greenstein et al 1989) than the red ^ green system and even in non-specific afflictions, the much lower density of S cones may be more disruptive for some tasks than any parvocellular loss. In such a case, the use of blue filters may be useful for two reasons. (i) They could help the remaining K cells to be better activated, if normally the K input to the dorsal stream assists in focal attention. (ii) They could reduce the activation of the P system. With the postulated severe loss of M cells, there may indeed be a significant degree of P encroachment into M targets in layers 4C and 2/3. Consequently, the latencies of the surviving M inputs and those of the P inputs would be very different, which could be as much as 30 ms in layer 4C (Nowak et al 1995). Furthermore, the receptive field loci of the contaminating P inputs could be sufficiently different from those of the M cells to add to the difficulties in sequential focusing of attention. The above scheme has predictable outcomes for the two groups with regard to their sensitivity to blue stimuli. The yellow-choosers, with presumably a larger cortical volume devoted to blue ON inputs, could exhibit an enhancement of blue sensitivity. This has in fact been observed by Dain and Floyd (2003), who found that increment thresholds for the blue ^ yellow system were significantly lower in the dyslexic group than in the normal. We do not know whether their subjects who showed significantly higher blue sensitivity were yellow-choosers. However, preliminary experiments by Stein's group (Stein 2003) showed that the blue-choosers were much less sensitive to S-cone modulation in a motion task than controls. 5 Conclusions The long history of evidence for a visual magnocellular deficit in dyslexia has also been matched by the evidence for an important role for phonological factors in the aetiology (eg Shaywitz 1996; Ramus et al 2003). However, the defect that leads to a visual magnocellular impairment may well be part of a more general deficit of all magno cells, leading to a temporal processing deficit affecting both visual and auditory systems (Tallal et al 1993; Stein and Walsh 1997). This may mean that phonological awareness could be independently affected, but the defects following a visual magnocellular impairment would lead to degraded inputs arriving at the processing stations concerned with the grapheme ^ phoneme conversion and aggravate the problems in subsequent auditory processing and word identification. The scheme proposed here provides a physiological basis for many testable predictions. For example, the inappropriate expansion of parvocellular or koniocellular inputs into the magno targets in the dorsal stream would affect visual search in different ways. The results of visual search employing red ^ green or blue ^ yellow stimuli and testing of S-cone sensitivity should be able to predict whether a yellow or blue filter would improve the reading score in dyslexics on an individual basis. However, at best, the overlays may only help in reducing the spatiotemporal interference of the attentional gating required in reading, but the basic magnocellular defect would be expected to impair reading, since the normal density and speed of spatial sampling at the critical visual field locations needed in reading cannot be achieved. Acknowledgments. I thank Paul Martin for helpful criticism of the manuscript, John Stein and Nicola Ray for permitting me to refer to their ongoing work and for many discussions, and the Australian National Health and Medical Research Council for supporting my work on visual attention and dyslexia.

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