Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2011 Sep 8.
Published in final edited form as: Vision Res. 2008 Apr 28;48(26):2682–2688. doi: 10.1016/j.visres.2008.03.005

First and second-order-motion perception after focal human brain lesions

Matthew Rizzo 1, Mark Nawrot 3, JonDavid Sparks 2, Jeffrey Dawson 2
PMCID: PMC3169341  NIHMSID: NIHMS80282  PMID: 18440580

Abstract

Perception of visual motion includes a 1st-order mechanism sensitive to luminance changes and a 2nd-order motion mechanism sensitive to contrast changes. We studied neural substrates for these motion types in 142 subjects with visual cortex lesions, 68 normal controls and 28 brain lesion controls. On 1st-order motion, the visual cortex lesion group performed significantly worse than normal controls overall and in each hemifield, but 2nd-order motion did not differ. Only 1 individual showed a selective 2nd-order motion deficit. Motion deficits were seen with lesions outside the small occipitotemporal region thought to contain a human homolog of motion processing area MT (V5), suggesting that many areas of human brain process visual motion.

Keywords: area MT, occipital lobe, visual cortex

1. Introduction

Much of what we know about the organization of the human visual system comes from studies of patients with brain lesions. During WW1, Holmes (1918) used skull x-rays showing entry and exit of missiles in soldiers with occipital wounds to infer a point-to-point map of the retina along the banks of the calcarine fissure of the occipital lobes (a.k.a., primary visual cortex, or area V1). Inouye (1909) made similar observations in soldiers injured in the Boxer Rebellion of 1900 and Russo-Japanese war of 1905. In addition to area V1, comparative anatomical studies in primates show multiple secondary visual areas such as V2, V3, V4, and V5 (a.k.a., mediotemporal area, MT). These areas receive inputs from different retinal ganglion cells via parallel pathways thought to convey a particular class of visual information, and have been grouped into two main cerebral pathways within the heuristic framework of “two visual systems” (Ungerleider and Mishkin, 1982). Case studies in patients with focal brain lesions suggest that the human visual system shows a similar organization. In general, these studies ask if lesions to area A impair performance in Task 1 is much greater than Task 2. When lesions to Area B affect Task 2 is much greater than Task 1, there is now a double dissociation. A double dissociation suggests Task 1 and 2 are handled by separate systems or differing sets of neurons within the same system. In this vein, ventral pathway lesions affecting the inferior visual association and temporal lobe produce disorders of visual recognition, reading and color perception (visual agnosia, acquired alexia and achromatopsia) as in the cases described by Pokorny, Smith and colleagues (Rizzo, Smith, Pokorny, 1993). Lesions of dorsal and lateral structures in the visual cortex and adjacent parietal lobe can impair visually guided eye and hand control and attention (as in Bálint and hemineglect syndromes) and can impair motion perception (cerebral akinetopsia) as in the famous case of “motion blind” patient LM (Zihl, Von Cramton and Mai, 1983).

This study uses the lesion method to test processing of different motion cues. Perception of visual motion depends on processing of different physical cues by the human brain. First -order motion refers to a change in luminance over space and time, as when a shadow passes over the ground. Second-order motion perception requires a more complex mechanism sensitive to change in contrast, not just luminance (Chubb and Spurling, 1989), such as when the wind creates waves of movement over a grassy field. An ongoing debate concerns how distinct these two motion processes are (Vaina, Cowey, Kennedy, 1999). Evidence from human brain lesion cases, functional neuroimaging in normal human observers (e.g., Smith, Greenlee, Singh, 1998; Ashida, Lingnau, Wall, 2007) and neuronal recordings in primates (e.g., O'Keefe and Movshon, 1998) suggest that 1st and 2nd-order motion are processed separately in the human brain, a hypothesis tested in the current study.

A few studies have used human brain lesions to probe differential processing of 1st and 2nd-order motion perception. Vaina and Cowey (1999) reported permanent impairment of 2nd-order motion perception in the contralesional visual field in FD, who had a unilateral lesion near putative human cortical area MT (V5). First -order motion was normal. Vaina, Makris, Kennedy (1998) reported selective impairment of 1st-order motion in the contralesional visual hemifield of RD, who had a unilateral brain lesion centered on putative visual areas V2 and V3 in the medial occipital lobe. His perception of 2nd-order motion was unimpaired. The conclusion from these studies, that the perception of 1st-order and 2nd-order motion are mediated by regionally separate mechanisms from an early stage of cortical processing, was assessed by applying a neocortical parcellation method to MRI scans of the patients’ brains (Vaina, Cowey and Kennedy, 1999).

Greenlee and Smith (1997) reported a substantial overlap in the cortical areas involved in 1st and 2ndorder speed discrimination. They tested detection and discrimination of 1st-order and 2nd-order motion in 21 patients with unilateral lesions of the lateral occipital, temporal, or posterior parietal cortex and 14 comparison subjects. The patients showed slight increase in orientation thresholds and moderate increase in direction thresholds. Speed discrimination thresholds were significantly elevated with lesions around the superior-temporal and lateral-occipital cortex, more so for 1st-order stimuli than for 2nd-order stimuli.

Braun, Petersen, Schonle (1998) assessed deficits and recovery of 1st-order and 2nd-order motion perception in nine patients with brain lesions. Two showed elevated thresholds for all stimuli presented in the contralesional hemifield, while thresholds for ipsilesional targets were spared. Neither showed any selective deficit of 1st versus 2nd-order motion perception, but 2nd-order motion was more impaired. Their lesions reportedly included the motion area V5 (MT), which was spared in the other seven patients. One patient was re-tested during a 27-month post-lesional period and showed complete recovery for 1st and 2nd-order motion direction discrimination, and for detection of speed differences. Nawrot, Rizzo, Rockland (2000) reported a transient deficit of 1st and 2nd-order motion perception in human following a limited resection of right anterior right occipital gyrus and posterior sector of the inferior and middle temporal gyri in patient SF; the 2nd-order motion processing defects recovered earlier.

Ellemberg, Lewis, Defina (2005) reported that visual deprivation due to congenital cataracts in 19 young patients was associated with greater losses in 2nd-order than 1st-order motion perception. Smith, et al. (1998) assessed 1st and 2nd-order motion processing in human visual cortex using functional magnetic resonance imaging (fMRI). Results suggested 1st-order motion sensitivity arises in V1, that 2nd-order motion is 1st represented explicitly in V3 and VP, and that V5 (MT) (and perhaps V3A and V3B) further processes motion information, including integration of both orders of motion signals. Marcar, Xiao, Raiguel (1995) studied cerebral activation in non-brain damaged human observers in imaging studies comparing 1st , 2nd, and 3rdorder motion (fast moving kinetic boundaries) and found no difference between the different motion orders. Fast fMRI adaptation techniques (Ashida et al., 2007) showed direction-selective adaptation for 1st-order and 2nd-order motion in human MT/MST, but no cross-adaptation between the two motion types in MT/MST. There were similar findings in V3A. The patterns of adaptation were consistent with psychophysical measurements of detection thresholds in similar stimulus sequences and suggested that separate neural populations process 1st and 2nd-order motion.

The current study addresses the separability of 1st and 2nd-order processing mechanisms by studying the pattern of motion processing deficits in patients with focal brain lesions, as outlined below.

2. Methods

2.1. Subjects

2.1.1 Visual Cortex Subjects

We recruited 142 subjects with chronic focal stable brain lesions (of at least 6 months duration) and behavioral deficits (age range 20-86, median age 54.5, mean age 53.1, SD= 15.5 years) from a registry of patients in the Department of Neurology (Palca, 1990). CT/MR images of lesion anatomy were assessed with 3D image reconstruction (Damasio and Frank, 1992) or by plotting lesions on standard 2D templates (Damasio and Damasio, 1989). Of these 142 individuals, 61 subjects had right hemisphere lesions only, 59 subjects had left hemisphere lesions only, and 22 subjects had bilateral lesions. These lesions included the visual cortex in the occipital lobes, parietal lobes, and posterior portions of the temporal lobes. Brain lesions in these subjects were also divided into dorsal lesions (P01, P02, P03, P04, P05, P06, O02, O05) and ventral lesions (T03, T04, T05, T06, O01, O03, O04, O06, O07) based on the templates of Damasio (1989; Table A.1).

All subjects completed a battery of standardized neuropsychological tests assessing a range of cognitive functions (Eslinger, Damasio, Graff-Radford, 1984; Eslinger, Damasio, Benton, 1985) and were intellectually capable of performing the experimental tasks presented here. Fifty-five (38.7%) of the subjects had homonymous visual field defects (hemianopia or quadrantanopia) defined by dynamic (Octopus Goldmann Kinetic Perimetry; Haag Streit AG, Koeniz-Berne, Switzerland) or static automated perimetry (Humphrey Perimetry; Carl Zeiss Meditec, Dublin, CA). Subjects had no cataracts, retinopathy, or glaucoma to account for the defects. No participant had ocular motor paralysis, congenital amblyopia, hereditary color blindness of retinal origin, senile macular degeneration, or untreated cataract requiring surgery.

2.1.2. Brain Lesion Controls

Twenty-eight subjects were tested as part of a control group included subjects with brain lesions affecting non-target locations (e.g., frontal lobe) not expected to directly involved motion processing. Their ages (range 24-77, median age 57.0, mean age 56.4, SD= 13.1 years) did not differ significantly (p =0.35) from those of the visual cortex lesion group. Of these 28 individuals, 16 had right hemisphere lesions, 12 had left hemisphere lesions and none had bilateral lesions. None of the 28 brain lesion control subjects had a visual field defect.

2.1.3. Normal Controls

Sixty-eight subjects without brain damage (age range 20-81, median age 61.5, mean age 51.7, SD= 19.9 years) comprised the neurologically normal comparison group. The controls did not significantly different in age from the visual cortex lesion cases (P=.9555).

2.1.4. Subject Gender

Seventy nine lesion subjects (55.6%), 27 normal controls (39.7%), 15 brain damage controls (53.6%), and 121 total (50.8%) were men.

2.1.5. Subject Exclusion Criteria

Exclusion criteria for all subjects in this study included neurodegenerative disorders, acute medical illness, active depression, alcoholism, and toxic metabolic disorders. Informed consent was obtained in accord with institutional and federal guidelines.

2.2. Apparatus

2.2.1 Basic Visual Function

Visual acuity was tested with Sloan letters at near range using a Snellen card and at 20 feet range using a wall chart. Spatial contrast sensitivity (CS) was assessed using a Pelli-Robson Contrast Sensitivity Chart (Clement Clarke, Columbus OH), which provides a measure of low to medium spatial frequency sensitivity, i.e. near peak CS function.

2.2.2 Motion Perception Stimuli

First-order and 2nd-order motion perception were tested using random dot cinematogram (RDC) stimuli generated by a Macintosh computer and displayed on a monitor viewed at a distance of 57 cm. Motion was tested in each of 5 regions, the center (5 degrees eccentric towards the four corners of the display monitor).

First-order stimuli resemble those used to test primates with area MT lesions (Newsome and Paré, 1988) and the human “motion blind” subject LM (Rizzo, Nawrot and Zihl, 1995). Here the 1st-order stimuli comprised 150 small (2' × 2') black dots drawn within a 4° square region. Within this region, dots all moved at the same speed, but the direction of dot movement varied between conveying signal and noise motion direction information. Signal dots conveyed one of the four cardinal directions, which varied between trials. Noise dots could move in any direction, and obscured the direction of the signal dots. Dots could switch between conveying signal and noise information, but over the entire stimulus the proportion of signal and noise dots was preserved in each trial. The proportion of signal dots varied over trials in a method of constant stimuli. The goal was to determine the percentage of signal dots required for subjects to correctly identify signal direction in a four alternative forced choice paradigm.

All subjects completed this task with a dot speed of 11.1°/s. Sixty-nine subjects and 54 controls also performed the task at a dot speed of 3.3°/s. The selection of these two velocities was based on Newsome, Mikami & Wurtz (1986) who suggested that MT processing is responsible for the perception of motion at higher velocities (> 8°/s) whereas both MT and V1 are responsible for perception of motion at slower velocities. If true, a velocity dependent motion perception deficit might be the result. For each velocity, two different signal ranges were used to span the region of expected thresholds. The first used a range of 20% to 80% signal dots. The direction of signal dot motion is relatively easy to detect with these stimuli, allowing a threshold estimate for “motion blind” subjects. For example, the motion blind subject “LM” had a threshold near 40% signal (Rizzo et al, 1995), and most patients with motion perception deficits resulting from midline cerebellar lesions had thresholds above 35% signal (Nawrot and Rizzo, 1995). Subjects with supra-threshold performance in this 20% to 80% signal range were tested with a lower signal range of 5% to 35% signal. For most subjects thresholds fell within this lower signal range.

The 2nd-order motion stimulus relied on contrast reversals to define movement (see Nawrot et al, 2000). These motion stimuli comprised a random two-dimensional array of 4' × 4' min squares. Half of the squares in the 62 by 62 square array were randomly assigned to white and the remaining squares were assigned to black (Figure 1). Second-order motion was generated by reversing the luminance of a proportion of squares within sequential four column (or row) intervals in each successive RDC frame. For example, downward motion at 100% signal was created by reversing the contrast of all 248 squares in the top four rows of the stimulus in the first motion frame, rows 5 through 8 when creating the next RDC frame, and all squares in rows 9 through 12 for the next RCD frame. This pattern continued through all RDC frames. The speed of this 2nd-order motion was 17.8°/sec. The proportion of signal was controlled by varying the number of squares to which the luminance inversion was applied. For instance, 10% signal would correspond to a randomly selected set of 25 squares changing for each RDC frame, rather than all 248 squares in the 100% signal condition.

This definition of signal in the 2nd-order motion stimulus means the 1st-order and 2nd-order thresholds are not directly comparable. Indeed, normal observers have much lower thresholds in the 2nd-order task when defined as it here (Nawrot et al., 2000). Due to the lower expected thresholds, the signal ranges used for 2ndorder motion were 5% to 35% and 1% to 7%. Most of the subjects had second-order motion thresholds within the 1%-7% signal range.

2.3 Procedures

Both 1st and 2nd-order motion stimuli were presented with the same psychophysical paradigm. Subjects were instructed to fixate a small cross at the center of the monitor and to maintain fixation on that point throughout the trial. They were instructed to not shift their gaze when stimuli were presented in one of the regions. Observers initiated trials with a hand held button. Motion stimuli were presented for 195 msec in one of the five screen locations (excepting cases of visual field defects wherein stimuli were not presented). Subjects gave a verbal or gestural response that the experimenter entered in to the computer using a key press. Subjects were permitted to take breaks from testing.

To avoid any effect of fatigue on the (often elderly) subjects, testing of different signal ranges and different velocities often occurred on different days. As the lesion effects on perceptual ability was assumed to be stable, the effect of testing day on performance was assumed to be small compared to the effect of fatigue.

3. Results

3.1. Basic Visual Function

There were no significant differences between any of the groups in basic visual functioning (Table 1).

Table 1.

Basic Visual Function

Medians, Means (Standard Deviations)
Contrast Sensitivity Near Acuity (logMar) Far Acuity
Normal Controls 1.8, 1.8 (.15) .048, .100 (.130) .04, .057 (.121)
Lesion Group 1.95, 1.81 (.21) .016, .064 (.102) 0, .025 (.145)
BD Control Group 1.95, 1.86 (.12) .016, .048 (.071) -.05, -.03 (.108)
Open in a new tab

3.2 Motion Perception

For each observer, at each signal range and speed tested, thresholds were obtained in each stimulus presentation region by a probit analysis. Thresholds (in % signal) were determined from where the psychometric function crossed the 63% correct point. For many subjects the higher stimulus signal ranges (20%-80%) failed to provide a threshold estimate as the subject had supra-threshold performance across the range. In such cases the lower signal range provided the threshold. If more than one signal range provided a reasonable threshold estimate (a threshold estimate within the range of the signal % used) then the lowest threshold estimate was used.

An overall score for each observer was calculated from the average of all five stimulus presentation regions. Hemifield scores for each subject were constructed from the average of the two scores from each hemifield (central test region not included). Some subjects with visual system lesions could not perform tests in certain regions due to hemianopia or quadrantanopia. Performance scores for these abnormal regions were treated as missing data for subsequent analyses.

We assessed threshold differences between visual cortex lesion cases and the neurologically normal and brain damage control groups to test to address the following hypotheses: (1) Subjects with lesions in visual cortices perform worse in for both motion types compared to normal control subjects and brain damage control subjects, (2) Subjects with unilateral visual cortex lesions perform worse in the contralesional fields than in the ipsilesional fields for both motion types, (3) Subjects with brain lesions in dorsal visual cortical areas perform worse for both motion types compared to subjects with lesions in ventral visual cortical areas, and (4) 1st and 2nd-order motion processing abilities decline with advancing age.

3.2.1. Motion Perception Results

Table 2 summarizes results in the visual cortex lesion cases, brain damage control lesion cases and neurologically normal control cases.

Table 2.

Thresholds (%Signal) on Motion Tests in the Neurologically Normal Control Group, Visual Cortex Lesion Group and Brain Damage Control Group

Medians, Means (Standard Deviations) 1st-order 3.3°/s 1st-order 11.1°/s 2nd-order
Overall 19.2, 23.4 (12.5) n=123 16.5, 19.9 (9.9) n=210 5.7, 7.3 (7.6) n=140
Normal Controls (overall avg.) (N=68) 15.7, 17.5 (7.8) n=54 13.3, 14.7 (5.1) n=68 5.8, 7.3 (6.7) n=50
Visual Cortex Lesion Group
Lesion Group (overall avg.) (N=142) 26.0, 28.0 (13.6) n=69 18.6, 22.4 (10.7) n=142 5.6, 7.4 (8.1) n=90
Left-hemisphere lesion only (N=59) 33.2, 31.8 (14.7) n=22 17.4, 21.4 (11.6) n=59 5.2, 7.3 (9.3) n=35
Right-hemisphere lesion only (N=69) 22.0, 24.4 (12.3) n=36 19.4, 22.5 (9.6) n=61 4.7, 6.3 (5.6) n=42
Bilateral lesions (N=22) 31.3, 32.1 (13.1) n=11 20.6, 25.0 (11.1) n=22 7.3, 11.0 (10.7) n=13
Ipsilesional field 23.4, 27.3 (14.5) n=53 18.7, 22.0 (11.7) n=116 4.8, 7.2 (8.1) n=71
Contralesional field 21.9, 25.0 (14.2) n=37 18.1, 20.7 (9.8) n=91 4.7, 6.6 (7.7) n=55
Brain Damage Control Group
BD Control Group (overall avg.) (N=28) 17.7, 24.1 (17.3) n=4 17.2, 18.0 (5.3) n=28 4.8, 5.6 (3.1) n=9
Left-hemisphere lesion only (N=15) 31.7, 31.7 (24.9) n=2 20.1, 20.8 (6.5) n=12 6.1, 6.4 (3.4) n=4
Right-hemisphere lesion only (N=20) 16.5, 16.5 (6.7) n=2 16.0, 15.9 (2.9) n=16 4.8, 4.9 (3.1) n=5
Bilateral lesions (N=8) Deleted Deleted Deleted
Ipsilesional field 23.4, 27.0 (17.7) n=4 17.4, 18.9 (7.5) n=28 4.5, 5.9 (4.4) n=9
Contralesional field 13.9, 22.0 (17.6) n=4 17.1, 17.4 (4.9) n=28 5.5, 6.6 (3.8) n=9
Open in a new tab

The visual cortex lesion group performed worse than the neurologically normal controls on 1st-order motion tests overall at 3.3 d/s (P<.0001) and 11.1 d/s (P<0.0001), in the contralesional field at 3.3 d/s (P=0.0288) and 11.1 d/s (P<0.0001), and in the ipsilesional field at 3.3 d/s (P=0.0011) and 11.1 d/s (P<0.0001). On 2nd-order motion, the visual cortex lesion group did not perform worse than neurologically normal controls overall (P=0.7525), in the contralesional field (P=0.4239), or in the ipsilesional field (P=0.5784). (All p-values are from Wilcoxon ranksum test).

Within the visual cortex lesion group, performance in the contralesional field was not worse than in the ipsilesional field for 1st-order motion at 3.3d/s (P=0.2936) and 11.1d/s (P=.4276) and was worse for 2nd-order motion (P=.0191). (P-values from Wilcoxon signed rank test). Spearman correlations in the visual cortex lesion cases were strong between 1st-order motion processing threshold scores at both speeds for overall scores (r =0.847), contralesional scores (r=0.822) and ipsilesional scores (r=0.739) (P<0.0001, all cases). 2nd-order motion order scores in the visual cortex lesion cases correlated with 1st-order motion overall at 11.1 d/s (r= 0.411, P<.0001) and at 3.3 d/s (r=0.419, P=.0012). 2nd-order motion in the visual cortex lesion cases correlated with 1st-order motion in the ipsilesional field at 11.1d/s (r= 0.446, P<.0001) and 3.3d/s (r= 0.616, P<0.0001) but not in the contralesional field at 11.1d/s (r=.220, P=0.1071) or 3.3d/s (r=-0.026, P=0.895). These findings reflect a strong relationship between processing 1st-order motion at different speeds. They also reflect worse processing of 1st-order motion compared to 2nd-order motion in the contralesional field of human subjects with visual cortical lesions.

In visual cortex lesion cases 1st-order motion scores at 11.1 d/s in the contralesional field were higher (worse) with right-sided lesions (22.21 [9.4]) than with left-sided lesions (18.95[10.2]). (P=.0266). Otherwise there were no significant difference in scores on the 1st and 2nd-order motion tests between patients with left-sided lesions and right-sided brain lesions. There were also no significant differences in 1st or 2nd-order motion scores between dorsal visual cortex lesion cases (N=35) and ventral visual cortex lesion cases (N=55) and subjects who had combined dorsal and ventral lesions (N=52).

The visual cortex lesion group did not perform worse than the brain damage control group on 1st-order motion tests, overall at 11.1 d/s (P=.1443, Wilcoxon ranksum), in the contralesional field at 11.1 d/s (P=.3620), and in the ipsilesional field at 11.1 d/s (P=.4020). On 2nd-order motion, the lesion group did not perform worse than the brain damage controls overall (P=0.9369), in the contralesional field (P=0.40), or in the ipsilesional field (P=0.8251). Had we counted scores from the visually impaired (hemianopic and quadranopic) fields as defective rather than missing, the visual cortex lesion group would have performed significantly worse than the brain damage control group both overall and in the contralesional fields.

Although there were no age differences between groups, we did find strong effects of age on motion processing. Overall threshold scores increased (got worse) with age for 1st-order motion at 3.3 d/s (P<.0001) and at 11.1 d/s (P<.0001), and 2nd-order motion (P<0.0001) when keeping age continuous. (N=220)

To better understand the effects of visual cortex lesions on motion processing, we also examined outlier cases. 53 of the 142 visual cortex lesion cases had overall scores > 2 SD than the means of the neurologically normal control group on one of the motion tasks (Table 3). Of these 53, 47 had overall scores >2 SD than the means of the control group on the 1st-order motion test at 11d/s. 32 of the 53 outlier cases were also tested at 3.3 d/s. Of these 32, 20 had scores > 2 SD for 1st-order motion at both speeds, 6 were abnormal at 11.1d/s only, and 5 were abnormal on 3.3d/s only.

Table 3.

Visual Cortex Lesions Cases with Motion Threshold Scores >2SD above the mean of Neurologically Normal Controls

SEX Age CS 1st Order 11d/s 1st Order 3d/s 2nd Order Outlier 1st Ord 11d/s Outlier 1st Ord 3d/s Outlier 2nd Order Lesion Location Lesion Side
1232 F 79 1.65 50.00 50.00 15.76 1 1 0 V, D, other L
1699 M 71 1.65 50.00 46.40 12.50 1 1 0 D, other R
1976 M 62 0.45 50.00 1 0 0 V, D, other L
264 F 52 48.25 50.00 4.24 1 1 0 V, D, other L
2308 M 45 1.80 46.42 1 0 0 V, other B
513 M 46 1.95 45.81 48.23 1 1 0 V, D, other L
1645 M 69 44.80 30.86 1 0 0 V, D, other L
983 F 62 43.93 50.00 30.00 1 1 1 V, D, other L
1676 F 21 1.65 41.93 32.07 9.17 1 0 0 V, D, other R
1566 F 71 1.95 41.48 50.00 2.15 1 1 0 V, D, other L
1879 F 42 1.95 40.83 1 0 0 D, other R
2002 M 38 1.95 40.12 3.63 1 0 0 V, other R
2016 F 67 1.65 39.97 13.70 1 0 0 V, D, other L
2245 M 39 1.80 38.31 1 0 0 V, D, other R
559 M 36 38.04 39.54 3.02 1 1 0 V, D, other L
1377 M 63 1.95 37.79 39.40 12.46 1 1 0 V, D, other R
2282 M 21 1.65 37.61 1.00 1 0 0 V, other R
744 M 83 1.65 37.53 28.24 1 0 1 D, other R
1640 M 51 37.28 50.00 1 1 0 D, other R
1669 M 70 36.68 42.53 1 1 0 V, D, other R
2102 F 48 1.95 36.31 1 0 0 V, D, other L
2126 F 53 2.10 35.96 1 0 0 D, other R
1687 M 58 1.95 34.12 45.90 7.56 1 1 0 V, D, other L
1924 M 72 1.35 33.85 9.09 1 0 0 V, other R
1980 F 77 33.64 1 0 0 D, other R
F 24 1.95 33.48 29.82 2.26 1 0 0 V, other R
1374 M 51 1.65 33.48 46.40 9.21 1 1 0 V, D, other L
2232 F 54 1.65 33.44 43.62 1 0 1 V, D, other R
1130 F 56 1.95 33.15 1 0 0 D, other L
1320 M 70 33.12 29.09 1 0 0 V, other R
692 F 30 1.95 32.36 46.66 7.79 1 1 0 V, other R
1620 F 65 31.42 49.10 3.10 1 1 0 D, other R
2067 F 51 1.80 31.34 1.55 1 0 0 V, D, other L
1864 F 74 1.65 30.88 22.45 1 0 0 D, other R
2771 F 74 1.50 30.86 1 0 0 V, D, other R
2435 M 56 1.80 30.81 9.24 1 0 0 D, other L
1790 F 61 1.50 29.65 40.15 17.40 1 1 0 V, D, other L
1615 M 41 28.98 40.23 5.20 1 1 0 V, other L
1103 M 68 1.65 28.74 38.10 24.17 1 1 1 V, D, other R
1500 F 75 28.50 44.80 1 1 0 V, other L
2061 F 69 1.65 27.41 7.26 1 0 0 V, other L
615 F 71 1.50 27.10 35.57 18.03 1 1 0 V, other L
1673 M 74 1.95 26.95 1 0 0 V, other B
1760 M 50 1.95 26.68 1.00 1 0 0 D, other L
2012 F 58 1.80 25.87 21.24 4.52 1 0 0 V, other L
1207 M 63 1.80 25.72 38.81 6.57 1 1 0 V, D, other R
1637 F 55 1.95 25.48 1 0 0 D, other R
1737 M 67 1.65 24.06 45.01 7.57 0 1 0 V, other R
1619 F 40 23.47 38.93 11.90 0 1 0 V, D, other L
1362 M 68 1.65 23.23 34.44 8.06 0 1 0 V, other R
1395 M 66 18.13 45.35 11.32 0 1 0 V, D, other L
1428 M 68 16.49 34.16 0 1 0 V, other R
1312 F 68 1.80 15.01 22.89 48.70 0 0 1 V, other L
Open in a new tab

V=Ventral, D=Dorsal, other= a lesion in non-visual areas, L=left hemisphere, R=right hemisphere, 1= a motion threshold score 2 or more standard deviations above that of the neurologically normal control subject threshold, 0= a motion threshold score within 2 standard deviations of the neurologically normal control subject thresholds.

Five visual cortex lesion cases had scores > 2 SD than the mean on the 2nd-order of motion task. Of these 5, 4 had abnormalities of 1st-order motion processing and 1 (subject 1312) had a 2nd-order motion score >2 SD than the means of the neurologically normal control group without a comparable abnormality of 1st-order motion processing. This deficit was associated with ventral lesions (affecting cells OO1, OO3 and TO6).

Of the 53 lesion visual cortex lesion cases with overall scores >2 SD than the means of the neurologically normal control group on one of the motion tasks, 21 had left hemisphere lesions, 22 had right hemisphere lesions and 10 had bihemispheric lesions. Deficits in some of these cases were comparable in severity to those in patient LM (about 40% signal at threshold), though their lesions were unilateral (Table 3).

Elevated motion thresholds were seen with lesions consistent with the locus provided by functional neuroimaging studies for a human motion processing region. The maps of Orban, Van Essen and Vanduffel (2004, their figure 3, p.317) would place “MT+” (area MT and neighboring regions) primarily in OO4. Fifteen of 142 subjects with lesions of visual cortex had a lesion including OO4. Table 4 compares the motion thresholds in visual cortex lesion cases with an OO4 lesion, versus without an OO4 lesion. Eight individuals who had lesions of OO4 (subjects 264, 983, 1103, 1207, 1374, 1500, 1687, and 2061) performed 2 SD or more worse than neurologically normal controls on the motion perception tasks. Of these 8 individuals, 7 were outliers at both 1st-order motion speeds and 1 (subject 2061) was an outlier at 11d/s only, 2 performed at least 2SD worse that the normal controls on 2nd-order motion subjects (983, 1103) and none had an isolated deficit of 2nd-order motion. We also identified motion perception deficits with lesions that fell substantially outside OO4. These included 45 of the 53 motion threshold outliers with visual cortex lesions. In addition, 3 of the 28 brain damage control subjects were motion outliers (2 at 11 d/s only and 1 at both speeds on the 1st degree motion task); they had in common a lateral frontal lobe lesion.

Table 4.

Thresholds (%Signal) on Motion Tests in Cases with and without a Lesion of OO4

N Mean Std Median Min Max P-value
First order 11ds OO4 lesion
No 127 22.093 10.626 18.403 6.742 50 0.222
Yes 15 25.443 11.325 21.743 13.376 48.25
Second order
No 80 7.006 7.911 5.35 1 48.703 0.2895
Yes 10 10.18 9.617 7.412 1.112 30
First order 3.3ds
No 60 26.5 13.349 22.751 7.508 50 0.0253
Yes 9 37.824 11.419 39.398 17.97 50
First order 11ds
Contralesional No 86 20.529 9.76 17.793 8.43 50 0.4487
Yes 5 24.32 11.796 24.66 11.665 41.535
First order 11ds
Ipsilesional No 105 21.406 11.363 18.395 4.685 50 0.0749
Yes 11 28.187 13.517 26.18 15.035 50
First order 3.3ds
Contralesional No 36 24.66 14.187 21.228 5.025 50 NA
Yes 1 38.44 . 38.44 38.44 38.44
First order 3.3ds
Ipsilesional No 48 25.797 14.224 21.918 2.6 50 0.0232
Yes 5 41.995 8.333 42.95 31.97 50
Open in a new tab

4. Discussion

This is the largest study to date on the effects of human brain lesions on motion processing and contains greater numbers of subjects than in all previous reports combined. The results of this study of visual motion perception are compatible with the hypothesis that 1st and 2nd-order motion are processed separately in the human brain. Comparisons between subjects with visual cortex lesions in the occipital lobe and adjacent parietal and temporal areas and neurologically normal control subjects without brain lesions showed that 1storder motion was significantly impaired in the visual cortex lesions cases both overall and in each visual hemifield. This differs from the pattern we observed in 2nd-order deficits because 2nd-order motion was not significantly impaired overall, in the contralesional field, or in the ipsilesional hemifield. The lack of correlation between 1st-order and 2nd-order motion scores in the contralesional field are also compatible with worse processing of 1st-order motion compared to 2nd-order motion in the contralesional field of subjects with visual cortical lesions.

This study showed that unilateral lesions of visual cortex in the right or left hemispheres can disturb motion processing in both hemifields. Results are compatible with the findings of Schenk and Zihl (1997), who tested visual motion perception in 32 patients with mostly unilateral brain lesions. Three had severely impaired visual motion perception in their contralateral visual hemifield, similar to perceptual defects in V5 (MT) lesioned monkeys. Two of these three had a right-hemisphere lesion and one had a left-hemisphere lesion. The authors concluded that both hemispheres contain a functional equivalent of V5 (MT), which serves visual motion perception primarily in the contralateral visual hemifield. The authors tested 1st-order, but not 2nd-order motion perception.

While we found defective 1st-order motion processing in the contralesional fields of subjects with visual cortex lesions, it was not significantly different than in the ipsilesional fields, probably because of our conservative approach to testing in fields with quadrantanopic or hemianopic loss in visual sensitivity. Rather than counting performance in these fields as abnormal, we assigned missing scores. This conservative approach also made it more difficult to detect predicted differences in 2nd-order motion processing thresholds between visual cortex lesion cases and neurologically normal controls, and in first and 2nd-order motion processing between visual cortex lesion cases and brain damage controls. However, our conservative approach helped ensure that any motion processing abnormalities we found were not simply due to a “preprocessing” deficit of visual sensitivity. Visual acuity and spatial contrast sensitivity were similar in brain lesion cases and neurologically normal controls, also indicating that defective motion processing in this study is not explained by a low level defect of CS or visual acuity.

This study did not find particular evidence that lesions in the visual cortex of the right hemisphere impair motion processing of either type more than lesions in the visual cortex of the left hemisphere, except for 1storder motion processing at the faster speed in the contralesional fields. Moreover, we did not find significant differences in motion processing thresholds of either type between subjects who had lesions in dorsal visual cortical areas thought to process motion versus ventral visual cortical areas. Note that the delineation between dorsal and ventral areas remains ambiguous. Indeed, the maps of Orban, Van Essen and Vanduffel (2004) would appear to place are MT/V5 and neighboring regions (“MT+”) mostly in OO4, which we included as part of the ventral pathways using the templates of Damasio (1989). Even so, our analyses showed no differences in either direction. Further, when we analyzed the performance of outlier cases for 1st-order and 2nd-order motion, we did not find a predominance of right hemisphere versus left hemisphere cases or of dorsal versus ventral lesion cases. Of the 53 visual cortex lesion cases with overall motion threshold scores >2 SD above the control group norm, only 5 showed abnormal 2nd-order motion; of these 5, only one did not show a comparable defect of 1st-order motion.

1st-order and 2nd-order motion processing may begin separately before feeding into the same mechanism. Brain mechanisms that localize features in a visual scene can access 1st-order information from the retinal image, but 2nd-order information must be extracted from the retinal intensity distribution by nonlinear processing (Volz and Zanker, 1996). Our results suggest that such 2nd-order information is more robustly represented at central levels, less susceptible to brain injury, and more likely to recover in the chronic phase when we tested. This could reflect an arrangement whereby information on 2nd-order motion from each hemifield is processed in both hemispheres, possibly through V3 (e.g., Smith, et al., 1998) and interhemispheric connections (e.g, Wilson, Ferrera and Yo,1992).

In this study of 142 individuals with lesions in visual cortex, just one individual showed a selective 2ndorder motion deficit like Vaina's subject FD, but 22 had a 1st-order motion deficit like RD. The anatomical localization for 1st and 2nd-order motion processing is not a specific as described in FD and RD. Results are compatible with the neuroimaging results that many areas of human brain respond to visual motion. Culham, Dukelow, and Verstraten (2001), in a review of neuroimaging results in motion perception, suggest that there is network of motion processing areas in the brain that goes far beyond the MT/MST complex. Sunaert, Van Hecke, Marchal (1999) compared motion and flicker responses to show that motion processing areas occur in many different cortical locations from occipital to even the frontal lobes (Figure 1 in Culham et al., 2001, summarizes of these results). The current study suggests that lesions of many of these various cortical regions can have an impact on motion perception; motion perception deficits are not caused solely by lesions of a small region of occipito-temporal cortex.

Finally, although there were no significant age related differences between the groups in this study of motion processing, this study showed strong effects of aging on visual motion processing in line with other reports that aging can impair processing of low-contrast moving contours (Sekuler, Hutman, and Owsley, 1980), optical flow (Atchley and Andersen, 1998), heading (Warren et al, 1998), coherent motion amid background noise, and speed (Snowden and Kavahagh, 2006). Growing evidence suggests that these declines reflect degraded information handling in cortical areas. Old primates show delayed intracortical and intercortical transfer of information throughout visual area V2 and parts of visual area V1 (Wang, Zhou, Ma, 2005). These temporal impairments coincide with degraded intracortical inhibition reduction of gamma aminobutyric acid (GABA) that may be reversible with pharmacologic interventions (Leventhal, Wang, Pu, 2003), suggesting potential treatment for subjects with motion processing deficits caused by aging and brain lesions.

Figure.

Figure

Open in a new tab

Schematic depicting four frames from the 2nd-order motion stimulus. The first frame shows the random black and white squares (here 10 × 10, the actual stimulus 62 × 62 squares, see the Methods section for details). In subsequent frames the contrast of successive rows (or columns) of dots was reversed in a sequential fashion. Motion is perceived in the direction of the successive contrast reversal through the stimulus, indicated here by the grey rectangle. In this figure, 100% of the dots reverse contrast, and the direction of second order motion is downward.

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

References

  1. Ashida H, Lingnau A, Wall MB, Smith AT. fMRI adaptation reveals separate mechanisms for first- order and second-order motion. Journal of Neurophysiology. 2007;97:1319–1325. doi: 10.1152/jn.00723.2006. [DOI] [PubMed] [Google Scholar]
  2. Atchley P, Andersen GJ. The effect of age, retinal eccentricity, and speed on the detection of optic flow components. Psychology and Aging. 1998;13:297–308. doi: 10.1037//0882-7974.13.2.297. [DOI] [PubMed] [Google Scholar]
  3. Braun D, Petersen D, Schonle P, Fahle M. Deficits and recovery of first- and second-order motion perception in patients with unilateral cortical lesions. European Journal of Neuroscience. 1998;106:2117–2128. doi: 10.1046/j.1460-9568.1998.00224.x. [DOI] [PubMed] [Google Scholar]
  4. Chubb C, Sperling G. Two motion perception mechanisms revealed through distance-driven reversal of apparent motion. Proceedings of the National Academy of Science. 1989;86:2985–2989. doi: 10.1073/pnas.86.8.2985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Culham J, He S, Dukelow S, Verstraten FAJ. Visual motion and the human brain: What has neuroimaging told us? Acta Psychologica. 2001;107:69–94. doi: 10.1016/s0001-6918(01)00022-1. [DOI] [PubMed] [Google Scholar]
  6. Damasio H. Human Brain Anatomy in Computerized Images. Oxford University Press; New York: 1989. [Google Scholar]
  7. Damasio H, Damasio AR. Lesion Analysis in Neuropsychology. Oxford University Press; New York: 1989. [Google Scholar]
  8. Damasio H, Frank R. Three-dimensional in vivo mapping of brain lesions in humans. Archives of Neurology. 1992;49:137–143. doi: 10.1001/archneur.1992.00530260037016. [DOI] [PubMed] [Google Scholar]
  9. Ellemberg D, Lewis TL, Defina N, Maurer D, Brent HP, Guillemot JP, Lepore F. Greater losses in sensitivity to second-order local motion than to first-order local motion after early visual deprivation in humans. Vision Research. 2005;45:2877–2884. doi: 10.1016/j.visres.2004.11.019. [DOI] [PubMed] [Google Scholar]
  10. Eslinger PJ, Damasio H, Graff-Radford N, Damasio AR. Examining the relationship between computed tomography and neuropsychological measures in normal and demented elderly. Journal of Neurology, Neurosurgery & Psychiatry. 1984;47:1319–1325. doi: 10.1136/jnnp.47.12.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eslinger PJ, Damasio AR, Benton AL, Van Allen M. Neuropsychologic detection of abnormal mental decline in older persons. Journal of the American Medical Association. 1985;253(5):670–674. [PubMed] [Google Scholar]
  12. Greenlee MW, Smith AT. Detection and discrimination of first- and second-order motion in patients with unilateral brain damage. Journal of Neuroscience. 1997;17:804–818. doi: 10.1523/JNEUROSCI.17-02-00804.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmes G. Disturbances of vision by cerebral lesions. British Journal of Ophthalmology. 1918;2:353–384. doi: 10.1136/bjo.2.7.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inouye T. Die Sehstörungen bei Schussverletzungen der kortikalen Sehsphäre. Engelmann; Leipzig, Germany: 1909. [Google Scholar]
  15. Leventhal AG, Wang Y, Pu M, Zhou Y, Ma Y. GABA and Its Agonists Improved Visual Cortical Function in Senescent Monkeys. Science. 2003;300(5620):812. doi: 10.1126/science.1082874. [DOI] [PubMed] [Google Scholar]
  16. Marcar VL, Xiao DK, Raiguel SE, Maes H, Orban GA. Processing of kinetically defined boundaries in the cortical motion area MT of the macaque monkey. Journal of Neurophysiology. 1995;74:1258–1270. doi: 10.1152/jn.1995.74.3.1258. [DOI] [PubMed] [Google Scholar]
  17. Nawrot M, Rizzo M. Motion perception deficits from midline cerebellar lesions in human. Vision Research. 1995;35:723–731. doi: 10.1016/0042-6989(94)00168-l. [DOI] [PubMed] [Google Scholar]
  18. Nawrot M, Rizzo M, Rockland KS, Howard M. A transient deficit of motion perception in human. Vision Research. 2000;40:3435–3446. doi: 10.1016/s0042-6989(00)00177-2. [DOI] [PubMed] [Google Scholar]
  19. Newsome WT, Mikami A, Wurtz RH. Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion. Journal of Neurophysiology. 1986;55:1340–1351. doi: 10.1152/jn.1986.55.6.1340. [DOI] [PubMed] [Google Scholar]
  20. Newsome WT, Paré EB. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience. 1988;8:2201–2211. doi: 10.1523/JNEUROSCI.08-06-02201.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Keefe LP, Movshon JA. Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey. Visual Neuroscience. 1998;15:305–317. doi: 10.1017/s0952523898152094. [DOI] [PubMed] [Google Scholar]
  22. Orban GA, Van Essen DC, Vanduffel W. Comparative mapping of higher visual areas in monkeys and humans. Trends in Cognitive Sciences. 2004;8:315–324. doi: 10.1016/j.tics.2004.05.009. [DOI] [PubMed] [Google Scholar]
  23. Palca J. Insights from broken brains. Science. 1990;248:812–814. doi: 10.1126/science.2188359. [DOI] [PubMed] [Google Scholar]
  24. Riddoch G. Dissociation of visual perception due to occipital injuries, with especial reference to appreciation of movement. Brain. 1917;40:15–57. [Google Scholar]
  25. Rizzo M, Smith V, Pokorny J, Damasio AR. Color perception profiles in central achromatopsia. Neurology. 1993;43:995–1001. doi: 10.1212/wnl.43.5.995. [DOI] [PubMed] [Google Scholar]
  26. Rizzo M, Nawrot M, Zihl J. Motion and shape perception in cerebral akinetopsia. Brain. 1995;118:11051127. doi: 10.1093/brain/118.5.1105. [DOI] [PubMed] [Google Scholar]
  27. Schenk T, Zihl J. Visual motion perception after brain damage: I. Deficits in global motion perception. Neuropsychologia. 1997a;35:1289–1297. doi: 10.1016/s0028-3932(97)00004-3. [DOI] [PubMed] [Google Scholar]
  28. Schenk T, Zihl J. Visual motion perception after brain damage: II. Deficits in form-from-motion perception. Neropsychologia. 1997b;35:1299–1310. doi: 10.1016/s0028-3932(97)00005-5. [DOI] [PubMed] [Google Scholar]
  29. Sekuler R, Hutman LP, Owsley CJ. Human aging and spatial vision. Science. 1980;209:1255–56. doi: 10.1126/science.7403884. [DOI] [PubMed] [Google Scholar]
  30. Smith AT, Greenlee MW, Singh KD, Kraemer FM, Hennig J. The processing of first- and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). Journal of Neuroscience. 1998;18:3816–3830. doi: 10.1523/JNEUROSCI.18-10-03816.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sunaert S, Van Hecke P, Marchal G, Orban GA. Motion-responsive regions of the human brain. Experimental Brain Research. 1999;127:355–370. doi: 10.1007/s002210050804. [DOI] [PubMed] [Google Scholar]
  32. Ungerleider LG, Mishkin M. Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW, editors. Analysis of Visual Behavior. MIT Press; Cambridge, MA: 1982. [Google Scholar]
  33. Vaina LM, Cowey A. Impairment of the perception of second-order motion but not first-order motion in a patient with unilateral focal brain damage. Procedings of the Royal Society London - Series B: Biological Sciences. 1996;263:1225–32. doi: 10.1098/rspb.1996.0180. [DOI] [PubMed] [Google Scholar]
  34. Vaina LM, Cowey A, Eskew RT, Jr., LeMay M, Kemper T. Regional cerebral correlates of global motion perception: Evidence from unilateral cerebral brain damage. Brain. 2001;124:310–321. doi: 10.1093/brain/124.2.310. [DOI] [PubMed] [Google Scholar]
  35. Vaina LM, Makris N, Kennedy D, Cowey A. The selective impairment of the perception of first-order motion by unilateral cortical brain damage. Visual Neuroscience. 1998;15:333–348. doi: 10.1017/s0952523898152082. [DOI] [PubMed] [Google Scholar]
  36. Vaina LM, Cowey A, Kennedy D. Perception of first- and second-order motion: separable neurological mechanisms? Human Brain Mapping. 1999;7:67–77. doi: 10.1002/(SICI)1097-0193(1999)7:1<67::AID-HBM6>3.0.CO;2-K. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Volz H, Zanker JM. Hyperacuity for spatial localization of contrast-modulated patterns. Vision Research. 1996;36:1329–1339. doi: 10.1016/0042-6989(95)00234-0. [DOI] [PubMed] [Google Scholar]
  38. Wilson HR, Ferrera VP, Yo C. A psychophysically motivated model for two-dimensional motion perception. Visual Neuroscience. 1992;9:79–97. doi: 10.1017/s0952523800006386. [DOI] [PubMed] [Google Scholar]
  39. Wang Y, Zhou Y, Ma Y, Leventhal AG. Degradation of Signal Timing in Cortical AreasV1 and V2 of Senescent Monkeys. Cerebral Cortex. 2005;15:403–408. doi: 10.1093/cercor/bhh143. [DOI] [PubMed] [Google Scholar]
  40. Zihl J, Von Cramon D, Mai N. Selective disturbance of movement vision after bilateral brain damage. Brain. 1983;106:313–340. doi: 10.1093/brain/106.2.313. [DOI] [PubMed] [Google Scholar]

RESOURCES