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A few remarks on attention and magnocellular deficits in schizophrenia
ARTICLE IN PRESS
Neuroscience and Biobehavioral Reviews 32 (2008) 118–122 www.elsevier.com/locate/neubiorev
Review
A few remarks on attention and magnocellular deficits in schizophrenia Bernt Christian Skottuna, John R. Skoylesb,c, a
Skottun Research, Oakland, CA, USA Centre for Mathematics and Physics in the Life Sciences and Experimental Biology (CoMPLEX), University College London, London, UK c Centre for Philosophy of Natural and Social Science, London School of Economics, London, UK
b
Received 16 March 2007; received in revised form 4 June 2007; accepted 5 June 2007
Abstract In connection with schizophrenia, it has been proposed that the magnocellular system is specifically linked to the guiding of covert visual attention. The argument is that the magnocellular pathway provides input to the dorsal cortical stream which then projects back to area V1. We review problems with this model. (1) It requires that responses in the magnocellular system have a lead time over responses in the parvocellular system. However, measurements indicate that the actual response time difference between the two systems is small or negligible when entering the visual cortex. (2) Attention can be modified by stimuli that do not activate the magnocellular system. And, (3) lesions to area MT in the dorsal stream impair smooth pursuit eye movements, but not saccadic eye movements which are associated with shifts in attention. For these reasons, it is difficult to link attention defects in schizophrenia to potential magnocellular deficits. r 2007 Elsevier Ltd. All rights reserved. Keywords: Dorsal stream; Latency; Magnocellular; Attention; Schizophrenia
Contents 1. 2. 3. 4. 5. 6. 7.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . The magnocellular system . . . . . . . . . . . . . . . Relative magnocellular and parvocellular delay The koniocellular inputs. . . . . . . . . . . . . . . . . Additional issues . . . . . . . . . . . . . . . . . . . . . . Magnocellular deficits in schizophrenia . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction Schizophrenia has been proposed to be associated with deficits in the magnocellular system (Keri et al., 2002, 2004; Schechter et al., 2005; Butler et al., 2007). It has also been indicated that schizophrenia is linked to deficits in visual Corresponding author. Centre for Mathematics and Physics in the Life
Sciences and Experimental Biology (CoMPLEX), University College London, London, UK. Fax: +44 20 7955 6869. E-mail address: [email protected] (J.R. Skoyles). 0149-7634/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2007.06.002
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attention (Laurens et al., 2005). These have been hypothesized to have their origin in the magnocellular system (Laycock et al., 2007). We would like to comment on this proposal, particularly on the suggestion that the guiding of attention is specifically linked to the magnocellular system. 2. The magnocellular system The term ‘‘magnocellular system’’ refers to one out of three parallel subcortical visual streams, which in primates
ARTICLE IN PRESS B.C. Skottun, J.R. Skoyles / Neuroscience and Biobehavioral Reviews 32 (2008) 118–122
can be traced from the retina through the lateral geniculate nucleus to the input layers of the primary visual cortex (V1). The other two streams are the parvocellular and the koniocellular systems (Shapley and Perry, 1986; Merigan and Maunsell, 1993; Hendry and Reid, 2000). The main difference between the three streams is that the parvocellular and koniocellular systems carry color information whereas the neurons in the magnocellular system have broadband tuning with regard to wavelength. In the visual cortex, there is considerable mixing of the inputs from the three subcortical systems (Lachica et al., 1992; Martin, 1992; Merigan and Maunsell, 1993; Sincich and Horton, 2005). Starting in the primary visual cortex two cortical streams— the dorsal and ventral streams—can be differentiated. Originally, it was thought that these two streams represented continuations of the magno- and parvocellular systems (Livingstone and Hubel, 1987). But more recent research has shown the situation to be more complex, and that the dorsal and ventral streams cannot be characterized as a simple continuations of the subcortical systems (Merigan and Maunsell, 1993; Skottun and Skoyles, 2006c). For instance, it has been shown that lesions placed in the magno- and parvocellular layers of the lateral geniculate nucleus have about equally strong effects on neurons in area V4 of the ventral stream (Ferrera et al., 1994). This indicates the presence of a strong magnocellular input to the ventral stream, i.e. an input which is strong at least in terms of function. With regard to the dorsal stream, it has been shown that it (i.e. area MT) receives a substantial direct koniocellular input (Sincich et al., 2004) as well as a sizable parvocellular input (Nassi et al., 2006). It has been found that later cortical stages project back to earlier ones (Shipp and Zeki, 1989). It has been proposed that such projections play a role in attention. Specifically, it has been proposed that magnocellular input to V1 is conveyed to the dorsal stream (also known as the parietal stream) from where it is projected back to cortical area V1, and that this feedback serves to direct covert visual attention (i.e. visually driven attention). For example, Laycock et al. (2007, p. 370) with regard to schizophrenia have suggested that ‘‘fast magnocellular inputs from V1 through the dorsal stream feedback into V1 where the re-entrant signal can integrate with the arrival of the parvocellular connections from LGN’’, and that this feedback to V1 serves to guide attention. A similar theory was proposed by Vidyasagar (1999, 2004) within the context of dyslexia (for an alternative perspective upon attention and magnocellular activity in relation to dyslexia, see Skottun and Skoyles, 2006a, b, 2007a, b). Central to these models is the idea that magnocellular activity is faster than the parvocellular activity giving the responses in the dorsal stream sufficient time to be transmitted back to V1 by the time the corresponding parvocellular responses arrived at this location. 3. Relative magnocellular and parvocellular delay The model of Laycock et al. (2007), therefore, depends critically upon there being a sufficient latency difference
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between the magno- and parvocellular responses (at the level of the visual cortex V1). The supposed latency difference between the two systems has been referred to as a ‘‘magnocellular advantage’’ (Maunsell et al., 1999; Laycock et al., 2007). Measurements, however, have found the average latency difference to be less than 10 ms (Marrocco, 1976; Maunsell et al., 1999; Maunsell and Gibson, 1992), and possibly as small as 5.5 ms (Nowak and Bullier, 1997). These values are with regard to the responses of single neurons. However, the parvocellular stream has about 10 times as many neurons as the magnocellular stream (Ahmad and Spear, 1993; Peters et al., 1994), which can make the latency difference between the two systems even smaller if the inputs from many cells ‘‘converge’’ (Maunsell et al., 1999). Maunsell et al. (1999) simulated such convergence and concluded that ‘‘convergence in cortex could eliminate or reverse the magnocellular advantage’’ (Maunsell et al., 1999, p. 1). The work of Valberg and Rudvin (1997) points to a similar conclusion. These authors plotted human VEP amplitudes as a function of contrast and identified two branches, one below about 10–20% contrast, and a second one at higher contrasts. The two branches were linked to inputs from the magno- and parvocellular systems, respectively. Valberg and Rudvin (1997) also plotted the response times of the amplitudes as a function of contrast. These plots do not show an abrupt discontinuity between the two branches, which indicates that the response times of the magno- and parvocellular inputs at the level of the visual cortex are similar. The work of Valberg and Rudvin (1997) also shows that the response time varies with contrast suggesting that the time difference between magno- and parvocellular response may also vary with contrast. The effect of contrast has also been documented in psychophysical experiments. Murray and Plainis (2003) concluded that psychophysical response times below about 10% contrast reflect magnocellular mechanisms and that the response times above this contrast level reflect parvocellular inputs. This finding indicates that the parvocellular system has a shorter latency than the magnocellular system at medium and high contrasts. These authors accounted for this observation in terms of a process by which ‘‘[i]ncreasing the contrast of the stimulus, recruits additional neurons (the more numerous P cells) and thus reduces synaptic delay’’ (Murray and Plainis, 2003, pp. 2714–2715). The findings of Murray and Plainis (2003), along with the findings of Valberg and Rudvin (1997), indicate that it may be inappropriate to specify latency values without making reference to contrast. It may therefore be the case that a sufficient magno-/parvocellular latency difference exists for the model proposed by Laycock et al. (2007) to function at low contrasts but not at high contrasts. It seems, however, that one would not want to adopt a model which could potentially work at low contrasts but not at high ones given that, as far as we understand, the attentional impairments of those with schizophrenia are not confined to low contrast levels.
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There is also evidence from VEP recordings to indicate that responses attributable to parvocellular inputs occur before responses of magnocellular origin. Ellemberg et al. (2001) associated the P1 and N1 peaks, respectively, with the magno- and parvocellular systems and noted that the N1 peak appeared before the P1 peak. This would suggest a shorter latency on the part of the parvocellular system. Similar observations have been made by Previc (1988) and Hammarrenger et al. (2003). Based on the above considerations, it is not clear that the responses of the magnocellular system would have sufficient time advantage over the responses from the parvocellular system to be able to travel to the parietal cortex and then down again to area V1 before the corresponding parvocellular inputs arrive. 4. The koniocellular inputs In this discussion, we have not considered the latencies of the koniocellular neurons. The response times of koniocellular neurons have not been studied extensively, but (based on recordings in bushbabies) it appears that these neurons are relatively slow (Hendry and Reid, 2000). However, should it turn out that these cells are faster than currently believed, the model of Laycock et al. (2007) may face a further obstacle. In this connection, it should be kept in mind that it has been established that there exists a fairly substantial mainly koniocellular direct input (i.e. an input bypassing V1) from the LGN to cortical area MT in the dorsal cortical stream (Sincich et al., 2004). Sincich et al. (2004) suggested that the small latency difference between MT and V1 responses may be the result of this direct koniocellular input to MT. This opens for the possibility that there may be early responses of koniocellular origin in the dorsal stream. If so, this would make it even more difficult to attribute early dorsal stream responses specifically to the magnocellular system. 5. Additional issues Another problem facing the proposal of Laycock et al. (2007) is that several studies have indicated that nonmagnocellular mechanisms may serve to guide attention (Sumner et al., 2002; Cole et al., 2005). Particularly, isoluminant color stimuli have been found to do so (Snowden, 2002). This seems to be at odds with a magnocellular mechanism since the magnocellular system has little sensitivity to isoluminant stimuli. Yet another problem is that Newsome et al. (1985) found that lesions to area MT resulted in deficiencies in smooth pursuit eye movements but not in saccadic eye movements. This appears to be at odds with the suggestion that this cortical area is an attentional mechanism since attention is closely linked to the guiding of saccadic eye movements rather than smooth pursuit movements. The model of Laycock et al. (2007) parallels the one of Vidyasagar (1999, 2004) in linking attentional defects to impairments in the magnocellular system. Vidyasagar’s
model was introduced in part to address the issue of attention deficits in dyslexia. In the case of dyslexia, there is, however, evidence to indicate that attentional impairments are not linked to magnocellular deficits. Roach and Hogben (2004) assessed attention capabilities in dyslexic individuals by using a cuing paradigm and found that these individuals benefited less from cuing than did controls. This was attributed to reduced attentional capabilities on the part of the dyslexic individuals. However, the same individuals did not show reduced magnocellular sensitivity when tested using a flicker contrast sensitivity task, indicating that their reduced attention capacity is not associated with magnocellular deficits. Laycock et al. (2007) specifically suggests that the feedback from cortical area MT to V1 could provide a possible mechanism for attentional guiding in V1. However, the receptive fields of the neurons in area MT are very large and may span as much as 20–301 (Mikami et al., 1986). But it would seem that if attention is to be directed to particular points in the visual field, it would need input from neurons with a much higher spatial specificity than those in area MT. Also, area MT is generally implicated in the perception of coherent motion (Newsome et al., 1989) for which the large receptive fields in MT seem well suited. However, what the relationship may be between coherent motion, which involves integration of direction information over large areas, and attention, which involves directing resources to a particular localized spot, is not clear. 6. Magnocellular deficits in schizophrenia If schizophrenic individuals were suffering from a magnocellular deficiency, one would expect these individuals to have visual performance deficiencies consistent with such a deficit. But it is not clear that they do. Contrast sensitivity is the most reliable and sensitive psychophysical test of magnocellular sensitivity (Skottun, 2000). In the case of a magnocellular deficit, one would expect this to manifest itself at low spatial and/or high temporal frequencies (Skottun, 2000). When one, in order to facilitate the comparisons, re-plots the data from the various studies in a common standard log–log coordinate system one finds that the results do not generally fit these predictions. For instance, in two studies, Slaghuis (1998, 2004) found a uniform sensitivity reduction across all spatial frequencies (the reductions were more severe for negative-symptom groups than for positive-symptom groups). Similar results were obtained by Slaghuis and Thompson (2003). Also Keri et al. (2002) found roughly general reductions in sensitivity, and Keri et al. (2000) found no statistically significant difference between schizophrenic individuals and controls using a 0.5 c/deg grating modulated at 8 Hz. Neither did Keri et al. (2004) using circular spots as stimuli. Further, tests of temporal contrast sensitivity have shown general reductions in sensitivity (Slaghuis, 1998; O’Donnell et al., 2006). Chen et al. (2003) found mild reductions in temporal contrast sensitivity
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confined to low and medium temporal frequencies which is at odds with what would be expected from a magnocellular defect. Slaghuis (1998) determined temporal contrast sensitivity at two spatial frequencies (1.0 and 8.0 c/deg) and found larger sensitivity deficits at the higher spatial frequency. Again, the results do not fit a magnocellular deficiency. The only study which to our knowledge has given results consistent with a magnocellular deficit is that of Butler et al. (2005). Therefore, the majority of contrast sensitivity studies have not found evidence for magnocellular deficits in schizophrenic subjects. This undermines the hypothetical link between magnocellular deficits and attention deficits in schizophrenia. General reductions in contrast sensitivity may be consistent with deficient attention (Skottun and Skoyles, 2007b). But to link attentional deficiencies in schizophrenia specifically to the magnocellular system is problematic given, e.g. that Slaghuis (1998) found larger deficits for 8 c/ deg stimuli than for 1.0 c/deg ones, that Chen et al. (2003) found significant deficits at only medium temporal frequencies and that Keri et al. (2000) found no deficit to 0.5 c/deg stimuli modulated at 8 Hz. Also the findings, mentioned above, of attention being directed by stimuli to which the magnocellular system is insensitive or only minimally sensitive (Snowden, 2002; Sumner et al., 2002; Cole et al., 2005) undermine the notion of a link between magnocellular activity and attention. 7. Conclusion Our argument is not that schizophrenic subjects do not suffer from attentional problems. On the contrary, as we have just pointed out much of the data are consistent with such individuals having an attentional deficit (see also Laurens et al., 2005). Neither do we deny that there is feedback from higher cortical areas back to lower ones, or that such feedback plays a role in guiding attention since research suggest both occur (Shipp and Zeki, 1989; Lamme et al., 1998; Ito and Gilbert, 1999). Nor do we claim that the magnocellular system and/or the dorsal cortical stream play no role in guiding attention. For instance, it may well be that all parts of the visual system contribute to the guiding of attention in which case the magnocellular system as well as the dorsal cortical stream would be expected to play their parts. The point of the present comments is whether there is a specific link between attentional problems and the magnocellular system in schizophrenic individuals. Our conclusion is that to link attention specifically or exclusively to the magnocellular system in such individuals is difficult to reconcile with much of the presently available data. References Ahmad, A., Spear, P.D., 1993. Effect of aging on the size density, and number of rhesus monkey lateral geniculate neurons. Journal of Comparative Neurology 334, 631–643.
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Neuroscience and Biobehavioral Reviews 32 (2008) 118–122 www.elsevier.com/locate/neubiorev
Review
A few remarks on attention and magnocellular deficits in schizophrenia Bernt Christian Skottuna, John R. Skoylesb,c, a
Skottun Research, Oakland, CA, USA Centre for Mathematics and Physics in the Life Sciences and Experimental Biology (CoMPLEX), University College London, London, UK c Centre for Philosophy of Natural and Social Science, London School of Economics, London, UK
b
Received 16 March 2007; received in revised form 4 June 2007; accepted 5 June 2007
Abstract In connection with schizophrenia, it has been proposed that the magnocellular system is specifically linked to the guiding of covert visual attention. The argument is that the magnocellular pathway provides input to the dorsal cortical stream which then projects back to area V1. We review problems with this model. (1) It requires that responses in the magnocellular system have a lead time over responses in the parvocellular system. However, measurements indicate that the actual response time difference between the two systems is small or negligible when entering the visual cortex. (2) Attention can be modified by stimuli that do not activate the magnocellular system. And, (3) lesions to area MT in the dorsal stream impair smooth pursuit eye movements, but not saccadic eye movements which are associated with shifts in attention. For these reasons, it is difficult to link attention defects in schizophrenia to potential magnocellular deficits. r 2007 Elsevier Ltd. All rights reserved. Keywords: Dorsal stream; Latency; Magnocellular; Attention; Schizophrenia
Contents 1. 2. 3. 4. 5. 6. 7.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . The magnocellular system . . . . . . . . . . . . . . . Relative magnocellular and parvocellular delay The koniocellular inputs. . . . . . . . . . . . . . . . . Additional issues . . . . . . . . . . . . . . . . . . . . . . Magnocellular deficits in schizophrenia . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction Schizophrenia has been proposed to be associated with deficits in the magnocellular system (Keri et al., 2002, 2004; Schechter et al., 2005; Butler et al., 2007). It has also been indicated that schizophrenia is linked to deficits in visual Corresponding author. Centre for Mathematics and Physics in the Life
Sciences and Experimental Biology (CoMPLEX), University College London, London, UK. Fax: +44 20 7955 6869. E-mail address: [email protected] (J.R. Skoyles). 0149-7634/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2007.06.002
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attention (Laurens et al., 2005). These have been hypothesized to have their origin in the magnocellular system (Laycock et al., 2007). We would like to comment on this proposal, particularly on the suggestion that the guiding of attention is specifically linked to the magnocellular system. 2. The magnocellular system The term ‘‘magnocellular system’’ refers to one out of three parallel subcortical visual streams, which in primates
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can be traced from the retina through the lateral geniculate nucleus to the input layers of the primary visual cortex (V1). The other two streams are the parvocellular and the koniocellular systems (Shapley and Perry, 1986; Merigan and Maunsell, 1993; Hendry and Reid, 2000). The main difference between the three streams is that the parvocellular and koniocellular systems carry color information whereas the neurons in the magnocellular system have broadband tuning with regard to wavelength. In the visual cortex, there is considerable mixing of the inputs from the three subcortical systems (Lachica et al., 1992; Martin, 1992; Merigan and Maunsell, 1993; Sincich and Horton, 2005). Starting in the primary visual cortex two cortical streams— the dorsal and ventral streams—can be differentiated. Originally, it was thought that these two streams represented continuations of the magno- and parvocellular systems (Livingstone and Hubel, 1987). But more recent research has shown the situation to be more complex, and that the dorsal and ventral streams cannot be characterized as a simple continuations of the subcortical systems (Merigan and Maunsell, 1993; Skottun and Skoyles, 2006c). For instance, it has been shown that lesions placed in the magno- and parvocellular layers of the lateral geniculate nucleus have about equally strong effects on neurons in area V4 of the ventral stream (Ferrera et al., 1994). This indicates the presence of a strong magnocellular input to the ventral stream, i.e. an input which is strong at least in terms of function. With regard to the dorsal stream, it has been shown that it (i.e. area MT) receives a substantial direct koniocellular input (Sincich et al., 2004) as well as a sizable parvocellular input (Nassi et al., 2006). It has been found that later cortical stages project back to earlier ones (Shipp and Zeki, 1989). It has been proposed that such projections play a role in attention. Specifically, it has been proposed that magnocellular input to V1 is conveyed to the dorsal stream (also known as the parietal stream) from where it is projected back to cortical area V1, and that this feedback serves to direct covert visual attention (i.e. visually driven attention). For example, Laycock et al. (2007, p. 370) with regard to schizophrenia have suggested that ‘‘fast magnocellular inputs from V1 through the dorsal stream feedback into V1 where the re-entrant signal can integrate with the arrival of the parvocellular connections from LGN’’, and that this feedback to V1 serves to guide attention. A similar theory was proposed by Vidyasagar (1999, 2004) within the context of dyslexia (for an alternative perspective upon attention and magnocellular activity in relation to dyslexia, see Skottun and Skoyles, 2006a, b, 2007a, b). Central to these models is the idea that magnocellular activity is faster than the parvocellular activity giving the responses in the dorsal stream sufficient time to be transmitted back to V1 by the time the corresponding parvocellular responses arrived at this location. 3. Relative magnocellular and parvocellular delay The model of Laycock et al. (2007), therefore, depends critically upon there being a sufficient latency difference
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between the magno- and parvocellular responses (at the level of the visual cortex V1). The supposed latency difference between the two systems has been referred to as a ‘‘magnocellular advantage’’ (Maunsell et al., 1999; Laycock et al., 2007). Measurements, however, have found the average latency difference to be less than 10 ms (Marrocco, 1976; Maunsell et al., 1999; Maunsell and Gibson, 1992), and possibly as small as 5.5 ms (Nowak and Bullier, 1997). These values are with regard to the responses of single neurons. However, the parvocellular stream has about 10 times as many neurons as the magnocellular stream (Ahmad and Spear, 1993; Peters et al., 1994), which can make the latency difference between the two systems even smaller if the inputs from many cells ‘‘converge’’ (Maunsell et al., 1999). Maunsell et al. (1999) simulated such convergence and concluded that ‘‘convergence in cortex could eliminate or reverse the magnocellular advantage’’ (Maunsell et al., 1999, p. 1). The work of Valberg and Rudvin (1997) points to a similar conclusion. These authors plotted human VEP amplitudes as a function of contrast and identified two branches, one below about 10–20% contrast, and a second one at higher contrasts. The two branches were linked to inputs from the magno- and parvocellular systems, respectively. Valberg and Rudvin (1997) also plotted the response times of the amplitudes as a function of contrast. These plots do not show an abrupt discontinuity between the two branches, which indicates that the response times of the magno- and parvocellular inputs at the level of the visual cortex are similar. The work of Valberg and Rudvin (1997) also shows that the response time varies with contrast suggesting that the time difference between magno- and parvocellular response may also vary with contrast. The effect of contrast has also been documented in psychophysical experiments. Murray and Plainis (2003) concluded that psychophysical response times below about 10% contrast reflect magnocellular mechanisms and that the response times above this contrast level reflect parvocellular inputs. This finding indicates that the parvocellular system has a shorter latency than the magnocellular system at medium and high contrasts. These authors accounted for this observation in terms of a process by which ‘‘[i]ncreasing the contrast of the stimulus, recruits additional neurons (the more numerous P cells) and thus reduces synaptic delay’’ (Murray and Plainis, 2003, pp. 2714–2715). The findings of Murray and Plainis (2003), along with the findings of Valberg and Rudvin (1997), indicate that it may be inappropriate to specify latency values without making reference to contrast. It may therefore be the case that a sufficient magno-/parvocellular latency difference exists for the model proposed by Laycock et al. (2007) to function at low contrasts but not at high contrasts. It seems, however, that one would not want to adopt a model which could potentially work at low contrasts but not at high ones given that, as far as we understand, the attentional impairments of those with schizophrenia are not confined to low contrast levels.
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There is also evidence from VEP recordings to indicate that responses attributable to parvocellular inputs occur before responses of magnocellular origin. Ellemberg et al. (2001) associated the P1 and N1 peaks, respectively, with the magno- and parvocellular systems and noted that the N1 peak appeared before the P1 peak. This would suggest a shorter latency on the part of the parvocellular system. Similar observations have been made by Previc (1988) and Hammarrenger et al. (2003). Based on the above considerations, it is not clear that the responses of the magnocellular system would have sufficient time advantage over the responses from the parvocellular system to be able to travel to the parietal cortex and then down again to area V1 before the corresponding parvocellular inputs arrive. 4. The koniocellular inputs In this discussion, we have not considered the latencies of the koniocellular neurons. The response times of koniocellular neurons have not been studied extensively, but (based on recordings in bushbabies) it appears that these neurons are relatively slow (Hendry and Reid, 2000). However, should it turn out that these cells are faster than currently believed, the model of Laycock et al. (2007) may face a further obstacle. In this connection, it should be kept in mind that it has been established that there exists a fairly substantial mainly koniocellular direct input (i.e. an input bypassing V1) from the LGN to cortical area MT in the dorsal cortical stream (Sincich et al., 2004). Sincich et al. (2004) suggested that the small latency difference between MT and V1 responses may be the result of this direct koniocellular input to MT. This opens for the possibility that there may be early responses of koniocellular origin in the dorsal stream. If so, this would make it even more difficult to attribute early dorsal stream responses specifically to the magnocellular system. 5. Additional issues Another problem facing the proposal of Laycock et al. (2007) is that several studies have indicated that nonmagnocellular mechanisms may serve to guide attention (Sumner et al., 2002; Cole et al., 2005). Particularly, isoluminant color stimuli have been found to do so (Snowden, 2002). This seems to be at odds with a magnocellular mechanism since the magnocellular system has little sensitivity to isoluminant stimuli. Yet another problem is that Newsome et al. (1985) found that lesions to area MT resulted in deficiencies in smooth pursuit eye movements but not in saccadic eye movements. This appears to be at odds with the suggestion that this cortical area is an attentional mechanism since attention is closely linked to the guiding of saccadic eye movements rather than smooth pursuit movements. The model of Laycock et al. (2007) parallels the one of Vidyasagar (1999, 2004) in linking attentional defects to impairments in the magnocellular system. Vidyasagar’s
model was introduced in part to address the issue of attention deficits in dyslexia. In the case of dyslexia, there is, however, evidence to indicate that attentional impairments are not linked to magnocellular deficits. Roach and Hogben (2004) assessed attention capabilities in dyslexic individuals by using a cuing paradigm and found that these individuals benefited less from cuing than did controls. This was attributed to reduced attentional capabilities on the part of the dyslexic individuals. However, the same individuals did not show reduced magnocellular sensitivity when tested using a flicker contrast sensitivity task, indicating that their reduced attention capacity is not associated with magnocellular deficits. Laycock et al. (2007) specifically suggests that the feedback from cortical area MT to V1 could provide a possible mechanism for attentional guiding in V1. However, the receptive fields of the neurons in area MT are very large and may span as much as 20–301 (Mikami et al., 1986). But it would seem that if attention is to be directed to particular points in the visual field, it would need input from neurons with a much higher spatial specificity than those in area MT. Also, area MT is generally implicated in the perception of coherent motion (Newsome et al., 1989) for which the large receptive fields in MT seem well suited. However, what the relationship may be between coherent motion, which involves integration of direction information over large areas, and attention, which involves directing resources to a particular localized spot, is not clear. 6. Magnocellular deficits in schizophrenia If schizophrenic individuals were suffering from a magnocellular deficiency, one would expect these individuals to have visual performance deficiencies consistent with such a deficit. But it is not clear that they do. Contrast sensitivity is the most reliable and sensitive psychophysical test of magnocellular sensitivity (Skottun, 2000). In the case of a magnocellular deficit, one would expect this to manifest itself at low spatial and/or high temporal frequencies (Skottun, 2000). When one, in order to facilitate the comparisons, re-plots the data from the various studies in a common standard log–log coordinate system one finds that the results do not generally fit these predictions. For instance, in two studies, Slaghuis (1998, 2004) found a uniform sensitivity reduction across all spatial frequencies (the reductions were more severe for negative-symptom groups than for positive-symptom groups). Similar results were obtained by Slaghuis and Thompson (2003). Also Keri et al. (2002) found roughly general reductions in sensitivity, and Keri et al. (2000) found no statistically significant difference between schizophrenic individuals and controls using a 0.5 c/deg grating modulated at 8 Hz. Neither did Keri et al. (2004) using circular spots as stimuli. Further, tests of temporal contrast sensitivity have shown general reductions in sensitivity (Slaghuis, 1998; O’Donnell et al., 2006). Chen et al. (2003) found mild reductions in temporal contrast sensitivity
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confined to low and medium temporal frequencies which is at odds with what would be expected from a magnocellular defect. Slaghuis (1998) determined temporal contrast sensitivity at two spatial frequencies (1.0 and 8.0 c/deg) and found larger sensitivity deficits at the higher spatial frequency. Again, the results do not fit a magnocellular deficiency. The only study which to our knowledge has given results consistent with a magnocellular deficit is that of Butler et al. (2005). Therefore, the majority of contrast sensitivity studies have not found evidence for magnocellular deficits in schizophrenic subjects. This undermines the hypothetical link between magnocellular deficits and attention deficits in schizophrenia. General reductions in contrast sensitivity may be consistent with deficient attention (Skottun and Skoyles, 2007b). But to link attentional deficiencies in schizophrenia specifically to the magnocellular system is problematic given, e.g. that Slaghuis (1998) found larger deficits for 8 c/ deg stimuli than for 1.0 c/deg ones, that Chen et al. (2003) found significant deficits at only medium temporal frequencies and that Keri et al. (2000) found no deficit to 0.5 c/deg stimuli modulated at 8 Hz. Also the findings, mentioned above, of attention being directed by stimuli to which the magnocellular system is insensitive or only minimally sensitive (Snowden, 2002; Sumner et al., 2002; Cole et al., 2005) undermine the notion of a link between magnocellular activity and attention. 7. Conclusion Our argument is not that schizophrenic subjects do not suffer from attentional problems. On the contrary, as we have just pointed out much of the data are consistent with such individuals having an attentional deficit (see also Laurens et al., 2005). Neither do we deny that there is feedback from higher cortical areas back to lower ones, or that such feedback plays a role in guiding attention since research suggest both occur (Shipp and Zeki, 1989; Lamme et al., 1998; Ito and Gilbert, 1999). Nor do we claim that the magnocellular system and/or the dorsal cortical stream play no role in guiding attention. For instance, it may well be that all parts of the visual system contribute to the guiding of attention in which case the magnocellular system as well as the dorsal cortical stream would be expected to play their parts. The point of the present comments is whether there is a specific link between attentional problems and the magnocellular system in schizophrenic individuals. Our conclusion is that to link attention specifically or exclusively to the magnocellular system in such individuals is difficult to reconcile with much of the presently available data. References Ahmad, A., Spear, P.D., 1993. Effect of aging on the size density, and number of rhesus monkey lateral geniculate neurons. Journal of Comparative Neurology 334, 631–643.
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