Gamma-Band Activity and Coherence in Response to Familiar and Unfamiliar Faces in Infants At-Risk for Autism Spectrum Disorder

Background: Behavioral and neurofunctional assays of face processing in autism spectrum disorder (ASD) have revealed atypical processing and recognition of faces across the lifespan. Furthermore, electrophysiological studies of infants at high risk for autism (HRA) have demonstrated aberrant face and gaze processing within the first year of life.  Although a majority of these studies have investigated event-related potentials, examining event-related oscillatory dynamics provides a complementary source of information regarding neurophsyiological correlates of face processing. Of particular interest is the gamma band frequency; variations in gamma power, revealed via time-frequency analysis, are thought to represent synchronized activity of smaller neural networks whereas phase coherence between discrete regions may be necessary for large-scale integration of functionally-specialized cortical regions. 

Objectives: To examine event-related gamma band activity and coherence to familiar and unfamiliar faces in HRA and low risk comparison (LRC) infants across the first year of life (6-, 9-, and 12-months). 

Methods: HRA and LRC infants completed visits at 6 (HRA = 21; LRC = 23), 9 (HRA = 26; LRC = 31) and 12 (HRA = 27; LRC = 18) months of age.  EEG was recorded using high density electrode arrays (Geodesic Sensor Net), sampled at 250 Hz, and referenced to single vertex electrode. Data were segmented into 1200ms epochs (200ms pre- 1000ms post-stimulus onset), trial/artifact rejected, and re-referenced to average reference. Infants with fewer than 12 good trials per condition were excluded. Stimuli included images of the infant’s mother and an unfamiliar stranger presented for 500ms. Time-frequency analysis was conducted to examine gamma-band activity (30-50 Hz) in three regions of interest (ROI): frontal, central, and posterior electrode locations; coherence analysis examined phase coherence for gamma band for left and right hemisphere frontal-posterior electrode pairs.

Results: Preliminary time-frequency analysis showed significant main effect of hemisphere for the posterior ROI by 9 months (p<.05) with greater gamma activity in the right compared to left hemisphere, but no main effect of group nor interaction between group and any other factor. Coherence analysis revealed marginally significant group by hemisphere interactions at 6- and 12-months (ps<.1). At 6 months HRA infants showed increased right hemisphere gamma coherence compared to LRC infants; however, by 12 months LRC infants showed a significant shift in rightward asymmetry resulting in greater right compared to left hemisphere coherence (p<.1), whereas HRA infants showed no asymmetry of coherence values for left versus right hemisphere at one year.

Conclusions: For both groups right-lateralized gamma activity in response to faces was apparent by 9 months; however, only LRC infants showed a trajectory of increasing rightward lateralization of intrahemispheric coherence during the first year of life. In contrast, infants at risk for ASD showed an atypical pattern of increasing leftward lateralization of frontoposterior gamma coherence. These results are in accord with prior findings of aberrant neural synchrony in autism, rather than of region-specific neural dysfunction. Finally, the current study provides further evidence that emergence of atypical face processing for individuals with a family history of ASD may occur within the first year of life.