Parvocellular pathway impairment in autism spectrum disorder: Evidence from visual evoked potentials
Introduction
Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by deficits in social interaction and communication, as well as restricted and repetitive behaviors and interests (Frith & Happé, 2005). Individuals with ASD exhibit superior performance on processing fine details (Happé, 1996, Happé and Frith, 2006, Ishida et al., in press, Jolliffe and Baron-Cohen, 1997). ASD individuals with high IQ tend to be poor at processing global structure and motion perception (Bertone et al., 2003, Milne et al., 2002, Spencer et al., 2000). Two distinct hypotheses have been proposed regarding abnormal early processing of the visual system in ASD. Spencer et al. (2000) proposed a ‘pathway-specific’ hypothesis. This hypothesis proposes that ASD involves a dysfunctional magnocellular (M) visual pathway, but preserved functioning in the parvocellular (P) pathway, causing an elevated motion coherence threshold (the minimum number of coherently moving elements supporting direction discrimination at some criterion level of performance), but preserved form coherence threshold (the static analog of the motion coherence threshold). Bertone et al. (2003) proposed an alternative ‘complexity-specific’ hypothesis. They measured sensitivity to first-order (luminance-defined) and second-order (texture-defined) motion stimuli and found a decrease in performance for second-order motion only. They proposed that inefficient neuro-integrative functioning affects complex information analysis in autism, regardless of static or dynamic visual information. The authors also evaluated the function of sub-cortical visual processing using the flicker contrast sensitivity task, and concluded that sub-cortical visual processing was intact (Bertone and Faubert, 2006, Bertone et al., 2003, Bertone et al., 2005).
P and M are the two major parallel visual pathways in humans (Tobimatsu & Celesia, 2006). Both systems begin in the retina and project to the primary visual cortex (V1) via the lateral geniculate nucleus (LGN). The P pathway projects to area V4 via the P-blob (color) and P-inter-blob (form) pathways of V1, and visual information is subsequently sent to the inferior temporal cortex. The P-color pathway is important for analyzing color information and the P-form pathway for processing detailed form information. In contrast, the M pathway projects to area V5/MT and terminates in the posterior parietal cortex. The M pathway plays an important role in detecting motion and processing of global structure (Livingstone and Hubel, 1988, Tobimatsu and Celesia, 2006). These distinct features depend on the specific physiological characteristics of the P and the M pathways. The former is characterized by high spatial resolution, color sensitivity, low contrast sensitivity, and low temporal resolution, while the latter exhibits opposite characteristics of low spatial resolution, color insensitivity, high contrast sensitivity, and high temporal resolution (Livingstone and Hubel, 1988, Tobimatsu and Celesia, 2006). Based on the concept of parallel visual processing, it is possible that the atypical superior visual processing of fine detail (local structure) and the inferior global structure and impaired motion processing in ASD might be related to superior functioning of the P pathway (particularly, the P-form pathway) and dysfunction of the M pathway.
Visual evoked potentials (VEPs) are a useful experimental tool and have been extremely useful in studies investigating the physiology and pathophysiology of the human visual system, including the visual pathways and visual cortex (Regan, 1989, Tobimatsu and Celesia, 2006). VEPs can be used to detect abnormalities not only in patients with visual deficits, but also in patients without visual symptoms upon examination (Tobimatsu & Celesia, 2006). VEPs exist in two forms—transient and steady-state (Tobimatsu & Celesia, 2006). Based on the different stimulus selectivity of the P and M pathways, our group has performed a number of studies using VEPs with appropriate visual stimuli to evaluate the functioning of the parallel visual pathways in both healthy subjects and patients with various neurological disorders (Tobimatsu et al., 2004, Tobimatsu et al., 2006, Tobimatsu and Kato, 1998, Tobimatsu et al., 1999, Tobimatsu et al., 1995, Nakashima et al., 2008, Yamasaki et al., 2004). Transient VEPs at low temporal frequencies elicited by chromatic sinusoidal gratings with equal luminance and high spatial frequency are suitable for examining the P pathway at the lower levels within V1. This stimulus evokes a characteristic negative wave (Nl) with a peak latency around 120 ms. Conversely, steady-state VEPs at high temporal frequencies that use achromatic sinusoidal gratings with low contrast and low spatial frequencies are useful for evaluating the M pathway within V1. This stimulation induces a positive peak (P1) around 120 ms followed by steady-state responses (Gutschalk, Patterson, Rupp, Uppenkamp, & Scherg, 2002).
To date, no studies have utilized VEPs to examine the neural basis of the ‘pathway-specific’ and ‘complexity-specific’ hypotheses, the two major hypotheses that have been proposed on the basis of psychophysical measurements. In addition, elemental chromatic and achromatic stimuli have not been previously used to study the parallel visual pathways within V1. Therefore, we aimed to objectively evaluate the neural substrates of the atypical visual performance observed in ASD. Special attention was paid to lower-level processing (within V1) of the P and M pathways elicited by appropriate visual stimuli.
Section snippets
Participants
Twelve ASD participants, including two adolescents and 10 adults with high-functioning ASD (eight males and four females, aged 17–38 years, mean age 28.1 years), and 12 healthy control participants, including one adolescent and 11 adults with similar chronological age and sex ratios (seven males and five females, aged 19–36 years, mean age 26.3 years), were enrolled in the study. The ASD group included six individuals with Asperger's disorder, three with autistic disorder, and three with
Intellectual function
The ASD participants exhibited normal IQ (verbal IQ, 111 ± 19.2 [mean ± SD]; performance IQ, 110 ± 12.8; full-scale IQ, 112 ± 13.8). There were no significant differences in chronological age (t-test) and sex ratio (χ2 test) between the two groups.
Parvocellular function
In the trials designed to elicit P pathway activation, all participants correctly named the cartoon characters following VEP recording. This confirms that participants were attentive during the experiment. The numbers of trials rejected for α-activity were
Dysfunction of the parvocellular-color pathway in ASD
Chromatic stimuli with equal luminance do not stimulate M neurons. The mean N1 latency in response to chromatic stimuli in high-functioning adults with ASD was significantly longer than in the control group. The chromatic stimuli used in this study would be expected to preferentially activate the color pathway, but not the form pathway, since the form pathway preferentially responds to gratings with high spatial frequency and high contrast (Tobimatsu & Celesia, 2006). In accord with these
Conclusion
The current study revealed that high-functioning adolescents and adults with ASD displayed a dysfunctional P pathway and a preserved M pathway at lower levels of visual processing within V1. These neurophysiological findings offer partial support to the ‘complexity-specific’ hypothesis, but not for the ‘pathway-specific’ hypothesis. Furthermore, our results indicated that color-processing abnormalities are also involved in high-functioning ASD. The P-form pathway within V1 as well as
Acknowledgments
This work was supported by a grant from JST, RISTEX. We would like to thank Ms. Ikue Ijichi and Yuka Miyanaga for their technical contributions.
References (36)
- et al.
Vagaries of visual perception in autism
Neuron
(2005) - et al.
Scalp electrode impedance, infection risk, and EEG data quality
Clinical Neurophysiology
(2001) - et al.
Sustained magnetic fields reveal separate sites for sound level and temporal regularity in human auditory cortex
Neuroimage
(2002) - et al.
Electrophysiological evidence for sequential discrimination of positive and negative facial expressions
Clinical Neurophysiology
(2008) - et al.
Studies of human visual pathophysiology with visual evoked potentials
Clinical Neurophysiology
(2006) - et al.
An integrated approach to face and motion perception in humans
Clinical Neurophysiology
(2006) - et al.
Parvocellular and magnocellular contributions to visual evoked potentials in humans: Stimulation with chromatic and achromatic gratings and apparent motion
Journal of Neurological Sciences
(1995) - et al.
Electrophysiological correlates of associative visual agnosia lesioned in the ventral pathway
Journal of Neurological Sciences
(2004) DSM-IV: Diagnostic and statistic manual of mental disorders
(1994)- et al.
Residual motion perception in a “motion-blind” patient, assessed with limited-lifetime random dot stimuli
Journal of Neuroscience
(1991)
Circular statistics in biology
Demonstrations of decreased sensitivity to complex motion information not enough to propose an autism specific neural etiology
Journal of Autism and Developmental Disorders
Motion perception in autism: A “complex” issue
Journal of Cognitive Neuroscience
Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity
Brain
Color perception in children with autism
Journal of Autism and Developmental Disorders
Autism spectrum disorder
Current Biology
Studying weak central coherence at low levels: Children with autism do not succumb to visual illusions. A research note
Journal of Child Psychology and Psychiatry
The weak coherence account: Detailed-focused cognitive style in autism spectrum disorders
Journal of Autism and Developmental Disorders
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