Autism spectrum disorders (ASD) are pervasive developmental disorders characterized by deficits in a variety of social, communicative, and emotional behaviors (APA, 2004
; Carter, Davis, Klin, & Volkmar, 2005
; Hobson, 2005
; Tager-Flusberg, Paul, & Lord, 2005
; WHO, 1992
). In addition to these primary symptoms, there is substantial evidence for atypicalities in visual (see Simmons, et al., 2009
) and auditory perception (see Kellerman, Fan, & Gorman, 2005
; Mottron, Dawson, Soulières, Hubert, & Burack, 2006
). Most relevant to the current study, individuals with ASD have been shown to exhibit impairments in motion perception (see Milne, Swettenham, & Campbell, 2005
). To date, there are two main hypotheses regarding the origins of this motion perception deficit. The first hypothesis is based on some evidence that the impairment may be restricted to stimuli that require motion integration, e.g., random dot kinematograms (Pellicano, Gibson, Mayberry, Durkin, & Badcock, 2005
, but see Vandenbroucke, Scholte, van Engeland, Lamme, & Kemner, 2008
, for opposing evidence from moving plaid stimuli), and/or higher-level computation e.g., second-order motion (Bertone, Mottron, Jelenic, & Faubert, 2003
). Such findings are consistent with an “integration hypothesis”, which postulates that impaired motion perception in ASD lies in impaired ability to integrate perceptual information, specifically complex perceptual information, rather than representing a deficit in motion perception per se. In support of this hypothesis, several studies have reported that integration of certain types of static elements is compromised in individuals with ASD, although this effect may be restricted to individuals with Autistic Disorder, and not Asperger’s syndrome (Spencer & O'Brien, 2006
; Tsermentseli, O’Brien, & Spencer, 2008
, and see Del Viva, Igliozzi, Tancredi, & Brizzolara, 2006
; Kemner, Lamme, Kovacs, & van Engeland, 2007
, for negative findings).
An alternative hypothesis is that the deficit in motion perception reflects a true impairment in cortical motion detectors, for example, within the middle temporal area, MT (see Albright, 1993
for a review of MT), or within subcortical pathways that feed into cortical motion detectors. There are two main subcortical pathways from the retina to the cortex, the magnocellular (M) pathway and the parvocellular (P) pathway. In brief, these two pathways, which originate in the retinal ganglion cells of the retina and remain segregated through the lateral geniculate nucleus up into primary visual cortex, differ markedly in their response properties (see Dobkins & Albright, 2004
; Merigan & Maunsell, 1993
, for reviews). [There is also a third subcortical pathway, referred to as the koniocellular (K) pathway. A lot less is known about this pathway (see Dobkins, 2000
; Hendry & Reid, 2000
) and thus will not be discussed further here.] Because cortical motion detectors receive the bulk of their input from the M pathway (Maunsell, Nealey, & DePriest, 1990
), it has been proposed that the motion perception impairment in ASD may originate in atypicalities within the subcortical M pathway (McCleery, Allman, Carver, & Dobkins, 2007
; Milne, et al., 2002
; Plaisted, Swettenham, & Rees, 1999
). We refer to this hypothesis as the “M pathway hypothesis”.
A number of perceptual studies have investigated the integrity of the M and P pathways by measuring performance on visual stimuli/tasks that are thought to differentially activate the M and/or P pathways. One approach has been to measure luminance contrast sensitivity of sinusoidal gratings presented at specific combinations of spatial and temporal frequencies as M neurons are more sensitive than P neurons to low spatial and high temporal frequencies, whereas P neurons are more sensitive than M neurons to high spatial and low temporal frequencies (Merigan & Maunsell, 1990
; Schiller, Logothetis, & Charles, 1990
). An alternative approach is to measure luminance and chromatic (red/green) contrast sensitivity, as the response properties of the M and P pathways mean that they are preferentially tuned for luminance and chromatic stimuli respectively (see Dobkins, 2009
). Specifically, M neurons are more sensitive than P neurons to luminance contrast, and conversely, P neurons are more sensitive than M neurons to red/green chromatic contrast (Lee, Pokorny, Smith, Martin, & Valberg, 1990
; Shapley, 1990
; Smith, Pokorny, Davis, & Yeh, 1995
It should be noted, however, that whether these approaches truly (and perfectly) isolate the M and P pathways has been called into question (see Lennie & D'Zmura, 1988
; Skottun, 2000
, for reviews), for two reasons. First, lesion studies have shown that, at some spatio-temporal frequencies, both M and P pathway lesions impair luminance contrast sensitivity (Merigan & Eskin, 1986
; Merigan, Katz, & Maunsell, 1991
; Merigan & Maunsell, 1990
; Schiller, et al., 1990
). Second, there are about eight times as many P than M neurons, and thus while each individual P neuron may have lower luminance contrast sensitivity than each M neuron, probability summation across neurons may give the P pathway the upper hand on luminance contrast sensitivity. While we acknowledge that the dichotomy is not complete, it is nonetheless reasonable to assert that there exists a bias
for the P and M pathways to contribute to Luminance and Chromatic CS, respectively. As such, atypical chromatic contrast sensitivity can be interpreted as atypical P pathway processing, whereas atypical luminance contrast sensitivity may be due to atypicalities in either the M or the P pathway.
With these caveats in mind, there have been many studies that have attempted to investigate the integrity of the M and P pathways in individuals with ASD by measuring luminance contrast sensitivity across a range of spatial and temporal frequencies. For example, one study that adopted this approach (M pathway stimulus = 0.5 cpd, 6 Hz, P pathway stimulus = 6 cpd, 1 Hz), reported no differences in contrast sensitivity between individuals with ASD and typically developing (TD) controls, on either the M or the P pathway stimulus (Bertone, Mottron, Jelenic, & Faubert, 2005
, and see Pellicano, et al., 2005
for similar findings using only an M pathway stimulus). Bertone et al. (2005)
also presented participants with an orientation-identification task using grating stimuli that were masked with luminance-defined noise. They reported enhanced luminance contrast sensitivity in individuals with ASD on this task. Unfortunately, the spatiotemporal frequency of these stimuli (0.75 cycles/degree, 0 Hz), and the addition of the luminance noise, make it difficult to know whether this effect was M- or P-pathway related. Another study (M pathway stimulus = 0.5 cpd, 12.5 Hz, P pathway stimulus = 13.4 cpd, 2 Hz), likewise, found no difference in contrast sensitivity between individuals with ASD and TD controls on the M pathway stimulus, however, they did find reduced contrast sensitivity for the P pathway stimulus in children and adolescents with ASD (Davis, Bockbrader, Murphy, Hetrick, & O’Donnell, 2006
). In sum, contrary to the “M pathway hypothesis”, the results from these studies suggest that M pathway processing is intact in ASD (but see Plaisted & Davis, 2005
for a discussion of why the size of the stimuli in these previous studies may not have been optimal for assessing M pathway processing), and that, if anything, P pathway processing may be impaired.
Luminance and chromatic contrast stimuli have yet to be employed for investigating M and P pathway processing in individuals with ASD, but we have recently used these stimuli in a forced-choice preferential looking study of 6-month-old infants who are at risk for developing ASD (McCleery, et al., 2007
). These infants are referred to as “high-risk” for ASD because they are thought to carry some of the genes for ASD since they have an older sibling diagnosed with the disorder (see Zwaigenbaum, et al., 2009
, for the logic behind the high-risk infant approach). In the study, we found that high-risk infants exhibited significantly higher luminance contrast sensitivity compared to “low-risk” control infants (from families without ASD history), yet typical chromatic contrast sensitivity. The luminance and chromatic stimuli were presented at a temporal frequency of 4.2 Hz, as infants were previously found to have optimal contrast sensitivity at this frequency (Dobkins, Anderson, & Lia, 1999
). The luminance stimuli employed in the study were presented at a very low spatial frequency of 0.27 cpd, making luminance contrast sensitivity measured in the study to be less likely to be mediated by the P pathway than the M pathway. Additionally, the P pathway is unlikely to be implicated in the higher luminance contrast sensitivity in the high-risk infants compared to the low-risk infants, as there was no difference in chromatic contrast sensitivity between the two infant groups, suggesting typical P pathway functioning in the high-risk infants. These results therefore suggest atypical (and enhanced) M pathway functioning associated with ASD, which we suggest could have negative repercussions on the developmental of those areas of the brain that are innervated by the M pathway (see Discussion). A difference score between luminance and chromatic contrast sensitivity was also calculated in the study, and compared between groups. The high-risk infants showed higher luminance vs. chromatic contrast sensitivity than the low-risk infants, who showed lower luminance vs. chromatic contrast sensitivity. This result suggests that there is also a significant difference in the relative functioning of the M and P pathways in the high-risk infants as compared to the low-risk infants.
We more recently reported that the severity of this atypicality is the same for the vast majority of our high-risk infants who did not go on to develop ASD as it is for the smaller percentage that did go on to develop ASD (Dobkins, Carver, Price, & Akshoomoff, 2010
). Together, these findings suggest that atypical M pathway processing may be an endophenotype of ASD, i.e., it may represent a genetically-mediated risk variable that is carried in both individuals with ASD and their first degree relatives (see Gottesman & Gould, 2003
; Gottesman & Sheilds, 1972
; Szatmari, et al., 2007
In sum, the results of previous contrast sensitivity studies investigating the integrity of M and P pathway processing in ASD have been somewhat mixed; studies of children/adults with ASD, which employed differing spatial/temporal frequencies, suggest no M pathway deficit (yet a possible P pathway deficit), while our previous study of high-risk infants, which employed luminance and chromatic stimuli, suggests possibly enhanced M pathway processing associated with ASD. There are at least three possible methodological reasons for the discrepancies across studies. First, the differences could be due to the different methodologies employed for distinguishing M and P pathway function (spatiotemporal frequency vs. luminance/chromatic). Second, the differences could be due to the different age groups tested (children/adults vs. infants). Third, the differences could be due to the different diagnostic status of the participants (diagnosed with ASD vs. having a sibling diagnosed with ASD).
Thus, the first goal of the current study was to control these differences across studies by obtaining luminance and chromatic contrast sensitivities in adolescents with ASD, as well as their “unaffected” adolescent siblings (SIBS) using the stimuli we employed in our previous high-risk infant study. Our decision to test SIBS was based both on wanting to compare them to our previously tested high-risk infants as well as wanting to investigate endophenotypes of ASD in adolescents, as this is becoming a strong and recognized approach to studying ASD (for example, Belmonte, Gomot, & Baron-Cohen, 2009
; Bolte & Poustka, 2003
; Dalton, Nacewicz, Alexander, & Davidson, 2007
; Dorris, Espie, Knott, & Salt, 2004
; Pellicano, 2008
). Specifically, if the effects we observed in high-risk infants persist into adolescence, we hypothesized that individuals with ASD and their SIBS would exhibit higher luminance contrast sensitivity than TD controls, indicative of atypical M pathway processing. Although, at first glance, this prediction would seem to go against the bulk of data showing no differences in luminance contrast sensitivity between ASD and TD individuals, as reviewed above, one paper has shown enhanced luminance contrast sensitivity in adults with ASD (Bertone, et al., 2005
), therefore we consider it important to measure luminance contrast sensitivity in a group of adolescents with ASD and also their unaffected SIBS.
The second goal of the current study was to examine decreased efficiency of motion processing in adolescents with ASD, as well as their SIBS, using a novel approach that controls for detectability. In the field of vision science, the “detection/motion” DET – MOT paradigm compares contrast sensitivity for detection of a moving grating stimulus (DET) to contrast sensitivity for direction-of-motion discrimination (MOT) of the same moving grating stimulus (Dobkins & Teller, 1996
; Graham, 1989
; Green, 1983
; Lindsey & Teller, 1990
; Palmer, Mobley, & Teller, 1993
; Watson, Thompson, Murphy, & Nachmias, 1980
). Here, a DET – MOT difference score of 0 indicates that contrast levels sufficient for detection of motion are sufficient for discriminating direction of motion, which suggests efficient motion processing. By contrast, a DET – MOT difference score greater than 0 indicates that contrast levels sufficient for detection of motion are not sufficient for discriminating direction of motion. This suggests inefficient motion processing, either because motion detectors are themselves impaired and/or because of reduced input from neural areas that project to motion detectors (see Dobkins, 2005
; Dobkins & Albright, 2004
, for review). This DET – MOT paradigm is especially valuable for studies of clinical populations, as one need to ensure that an impairment observed on a motion task is not simply a result of a lesser ability to detect the presence of the motion stimulus per se. The DET – MOT paradigm has the equally important benefit of determining whether an apparent lack of impairment on a motion task results from a combination of inefficient motion processing that is counteracted by an overall enhanced ability to simply detect the motion stimulus.
The DET – MOT paradigm measures direction discrimination abilities while controlling for stimulus detectability. An elevated DET – MOT difference score indicates inefficient motion processing, either because the motion detectors are themselves impaired and/or because of reduced input from neural areas that project to motion detectors. Given that there are numerous examples within the literature of impaired motion perception in ASD, we predicted that participants with ASD would exhibit higher DET – MOT difference scores than the TD controls. If inefficient motion processing is an endophenotype of ASD then we also expected to see higher DET – MOT difference scores in the SIBS group compared to controls. As described in the Discussion, by looking to see whether group differences on this metric were greater for luminance or chromatic stimuli, we hoped to differentiate between impairments in motion detectors vs. reduced input to motion detectors.