Rapid Sensorimotor Behaviors
Grip Force Accuracy
Probands showed greater force overshoot than TD controls at 15% MVC (d = 0.254), particularly at younger ages (group x age x MVC: β = 0.006, SE = 0.002, p = 0.001; Figure S1). This small but significant effect was driven by BAP- probands who showed greater force overshoot than BAP + probands (d = 0.206) and TD controls (d = 0.294) at 15% MVC at younger ages [group (BAP- vs TD control) x age x MVC: β = 0.007, SE = 0.002, p = 0.006; group (BAP + vs TD control) x age x MVC: β = 0.003, SE = 0.002, p = 0.219; BAP + vs BAP- at 15% MVC: t = 2.392, p = 0.029, Fig. 3).
Female parent controls showed greater force overshoot than proband mothers, though this was a small effect (d = 0.117). Proband fathers and male controls showed similar performance (group x sex: β=-0.020, SE = 0.008, p = 0.008; Figure S2). No differences between BAP + or BAP- parents and controls were seen for rapid force accuracy.
Saccade Accuracy
Probands showed greater saccade error relative to TD controls for 24-degree targets (d = 0.236; group x amplitude: β = 0.291, SE = 0.088, p < 0.001; Figure S3A). This difference was seen in both BAP+ (d = 0.278) and BAP- (d = 0.196) probands compared to TD controls [group (BAP- vs TD control) x amplitude: β = 0.237, SE = 0.118, p = 0.044; group (BAP + vs TD control) x amplitude: β = 0.341, SE = 0.103, p < 0.001; Fig. 4A]. For leftward saccades, BAP- probands showed greater error compared to TD controls [d = 0.103; group (BAP- vs TD control) x direction: β=-0.302, SE = 0.114, p = 0.008; group (BAP + vs TD control) x direction: β = 0.142, SE = 0.100, p = 0.154].
Proband parents showed increased saccade error relative to parent controls at 24-degrees (d = 0.084; group x amplitude: β = 0.094, SE = 0.043, p = 0.032; Figure S3B). BAP- parents showed greater error to 24-degree targets compared to BAP + parents (d = 0.095) and parent controls [d = 0.103; group (BAP- vs control) x amplitude: β = 0.135, SE = 0.046, p = 0.004; group (BAP + vs control) x amplitude: β=-0.030, SE = 0.058, p = 0.609; BAP + vs BAP- at 24-degrees: t=-2.140, p = 0.033; Fig. 4B].
Saccade Velocity
Probands demonstrated higher peak saccade velocities compared to TD controls, especially for leftward saccades (left: d = 0.326, right: d = 0.269; group x direction: β= -0.629, SE = 0.271, p = 0.002; Figure S4A). Both BAP+ (12°: d = 0.258, 24°: d = 0.486) and BAP- probands (12°: d = 0.684, 24°: d = 0.680) showed higher saccade velocity compared to TD controls, and BAP- probands showed higher saccade velocity than BAP + probands, especially for 12-degree targets [12°: d = 0.475, 24°: d = 0.240; group (BAP- vs TD control) x amplitude: β=-2.436, SE = 0.372, p < 0.001; group (BAP + vs TD control) x amplitude: β = 0.915, SE = 0.326, p = 0.005; BAP + vs BAP- at 12-degrees: t=-6.166, p < 0.001; BAP + vs BAP- at 24-degrees: t=-2.900, p = 0.004; Fig. 5A]. BAP + probands showed higher saccade velocity compared to TD controls only for leftward targets [d = 0.198; group (BAP- vs TD control) x direction: β=-0.097, SE = 0.358, p = 0.786; group (BAP + vs TD control) x direction: β=-0.751, SE = 0.312, p = 0.016].
Proband parents showed higher peak saccade velocity compared to parent controls, especially at 24-degrees (12°: d = 0.287, 24°: d = 0.304; group x amplitude: β= -0.501, SE = 0.185, p = 0.001; Figure S4B). BAP + parents showed increased velocity compared to parent controls (12°: d = 0.175, 24°: d = 0.250), and BAP- parents showed increased velocity compared to BAP + parents (12°: d = 0.181, 24°: d = 0.097) and parent controls (12°: d = 0.352, 24°: d = 0.347), particularly at 12-degrees [group (BAP- vs control) x amplitude: β=-0.544, SE = 0.197, p = 0.006; group (BAP + vs control) x amplitude: β=-0.425, SE = 0.249, p = 0.088; BAP + vs BAP- at 12-degrees: t=-4.258, p < 0.001; BAP + vs BAP- at 24-degrees: t=-2.067, p = 0.039; Fig. 5B].
Saccade Duration
Probands made saccades with shorter durations compared to TD controls (d = 0.266; β= -0.243, SE = 0.102, p = 0.020; Figure S5A). Both BAP+ (d = 0.248) and BAP- probands (d = 0.364) showed shorter saccade duration than TD controls, and BAP- probands showed shorter saccade duration than BAP + probands (d = 0.114; BAP- vs TD control: β=-0.419, SE = 0.139, p = 0.004; BAP + vs TD control: β=-0.267, SE = 0.120, p = 0.030; BAP + vs BAP-: t = 2.074, p = 0.038; Fig. 6A).
Proband parents showed shorter saccade durations compared to parent controls, particularly at 12-degrees (12°: d = 0.262, 24°: d = 0.213; group x amplitude: β = 0.118, SE = 0.036, p = 0.001; Figure S5B). BAP- parents demonstrated shorter saccade durations compared to BAP + parents (12°: d = 0.221, 24°: d = 0.264) and parent controls (12°: d = 0.329, 24°: d = 0.326) at 12 and 24 degrees; BAP + parents showed shorter saccade duration compared to controls only for 12-degree targets [d = 0.120; group (BAP- vs control) x amplitude: β = 0.112, SE = 0.0439, p = 0.004; group (BAP + vs control) x amplitude: β = 0.098, SE = 0.049, p = 0.045; BAP + vs BAP- at 12-degrees: t = 4.885, p < 0.001; BAP + vs BAP- at 24-degrees: t = 5.310, p < 0.001; Fig. 6B].
Sustained Sensorimotor Behaviors
Grip Force Variability
Probands showed increased force variability relative to controls (15% MVC: d = 0.160; 45% MVC: d = 0.263; 85% MVC: d = 0.222), especially at younger ages (group x age x MVC: β = 0.011, SE = 0.005, p = 0.047; Fig. 7A). Increased force variability was driven by BAP + probands who showed increased variability relative to TD controls (15% MVC: d = 0.172; 45% MVC: d = 0.386; 85% MVC: d = 0.407) and BAP- probands (15% MVC: d = 0.074; 45% MVC: 0.275; 85% MVC: d = 0.327), especially at higher force levels [group (BAP- vs TD control) x MVC: β=-0.006, SE = 0.007, p = 0.387; group (BAP + vs TD control) x MVC: β = 0.015, SE = 0.007, p = 0.025; BAP + vs BAP- at 45% MVC: t=-2.313, p = 0.021; BAP + vs BAP- at 85% MVC: t=-2.517, p = 0.013; Fig. 7B].
Proband parents showed greater force variability than parent controls at 85% MVC with their dominant hand (d = 0.378) and at 45% MVC with their non-dominant hand (d = 0.285; group x MVC x hand: β = -0.018, SE = 0.009, p = 0.044, Figure S6). Proband fathers showed greater variability relative to male parent controls at 85% MVC only (d = 0.275; group x MVC x sex: β=-0.019, SE = 0.009, p = 0.043). These findings were driven by BAP- fathers showing greater force variability than male parent control (45% MVC: d = 0.264; 85% MVC: d = 0.356) and BAP + fathers at higher force levels [45% MVC: d = 0.452; 85% MVC: d = 0.380; group (BAP- vs control) x MVC x sex: β=-0.028, SE = 0.010, p = 0.004; group (BAP + vs control) x MVC x sex: β = 0.0004, SE = 0.012, p = 0.976; BAP + vs BAP- males at 45% MVC: t = 3.600, p < 0.001; 85% MVC: t = 2.929, p = 0.004); Fig. 8A]. BAP- mothers showed greater force variability than female parent controls (d = 0.297) and BAP + mothers at 15% MVC [d = 0.280; (BAP + vs BAP- mothers at 15% MVC: t = 2.538, p = 0.012; Fig. 8B).
Smooth Pursuit Gain
The group x age interaction approached significance for pursuit gain reflecting a reduction in pursuit gain in probands relative to controls at younger ages (d = 0.018; β = 0.054, SE = 0.028, p = 0.065; Fig. 9A). BAP + probands showed reduced pursuit gain compared to BAP- probands (d = 0.410) and TD controls (d = 0.263) for rightward trials only [group (BAP- vs control) x direction: β = 0.056, SE = 0.312, p = 0.858; group (BAP + vs control) x direction: β=-0.797, SE = 0.278, p = 0.004; BAP + vs BAP for rightward trials: t=-3.845, p < 0.001; Fig. 9B]. No differences in pursuit gain were seen between proband parents and parent controls or between BAP + or BAP- parents and parent controls.
Familiality of Sensorimotor Deficits in Family Trios and Duos
Saccade velocity was highly intercorrelated among probands and their parents (h2 = 0.848, p < 0.001). Separate analyses for BAP + and BAP- families indicated that saccade velocity was familial across both groups (BAP+: h2 = 0.625, p = 0.036; BAP-: h2 = 0.953, p < 0.001); saccade duration was familial only for BAP- families (h2 = 0.557, p = 0.029). Precision gripping and pursuit outcomes were not familial.
Relationship Between Manual Motor and Oculomotor Behavior
For TD controls, increased rapid force overshooting at 15% MVC was related to increased saccade velocity (r = 0.579, p = 0.002; Table S3). For autistic individuals, increased pursuit gain was related to reduced grip force variability (r=-0.541, p = 0.002) and increased rapid grip force accuracy at 85% MVC (r = 0.522, p = 0.003). No other relationships between precision gripping and oculomotor outcomes were significant.
Clinical and Demographic Correlations
BAP + probands showed more severe parent-reported hyperactivity/impulsivity (t=-2.76, p = 0.01; Table 2) and trended toward showing more severe RBS-R rated ritualistic behaviors (t=-1.968, p = 0.056) and insistence on sameness (t=-1.946, p = 0.059) compared to BAP- probands. Neither precision gripping nor oculomotor impairments were related to ASD severity in probands or BAP features in parents (|r|’s ≤ 0.475; see Tables S4-S7).
Table 2
Demographic and clinical characteristics of probands and parents based on BAP status
| BAP + Probands (N = 22) | BAP- Probands (N = 23) | BAP+ Parents (N = 30) | BAP- Parents (N = 74) | |
% Malea | 95 | 91 | 43 | 49 | |
Age (years) | 11 (4) | 11 (3) | 41 (5) | 42 (6) | |
PIQ | 104 (20) | 100 (17) | 113 (11) | 110 (11) | |
VIQ | 93 (19) | 96 (20) | 111 (13) | 107 (11) | |
ADOS-2 CSS | 8 (2) | 8 (2) | | |
ADI-R Social | 23 (5) | 21 (6) | | | |
ADI-R Communication | 17 (5) | 17 (4) | | | |
ADI-R RRB | 6 (3) | 5 (2) | | | |
RBS-R – Total | 32 (16) | 23 (17) | | | |
RBS-R – Compulsive | 4 (5) | 3 (4) | | | |
RBS-R – Restricted | 4 (2) | 3 (2) | | | |
RBS-R – Ritualistic | 7 (4) ~ | 5 (4) | | | |
RBS-R – Sameness | 9 (5) ~ | 6 (5) | | | |
RBS-R – Self-Injurious | 2 (3) | 2 (2) | | | |
RBS-R – Stereotyped | 5 (3) | 4 (4) | | | |
Conners – Hyperactivity | 76 (11)** | 64 (14) | | | |
BAP-Q Self Total | | | 3.5 (0.6)*** | 2.4 (0.5) |
BAP-Q Self Aloof | | | 3.7 (0.8)*** | 2.5 (0.7) | |
BAP-Q Self Pragmatic | | | 3.0 (0.8) *** | 2.0 (0.5) | |
BAP-Q Self Rigid | | | 3.7 (0.8) *** | 2.6 (0.6) |
Note. Data are reported as mean and standard deviation in parentheses. a % Male was compared across groups using a chi-square test. PIQ = performance IQ; VIQ = verbal IQ; ADOS-2 = Autism Diagnostic Observation Schedule, Second Edition; RBS-R = Repetitive Behavior Scale-Revised; BAP-Q = Broad Autism Phenotype-Questionnaire. ***p < 0.001, **p < 0.01, ~p < 0.06. |