Varying stimulus duration reveals consistent neural activity and behavior for human face individuation

in Neuroscience (2021), 472

Establishing consistent relationships between neural activity and behavior is a challenge in human cognitive neuroscience research. We addressed this issue using variable time constraints in an oddball ... [more ▼]

Establishing consistent relationships between neural activity and behavior is a challenge in human cognitive neuroscience research. We addressed this issue using variable time constraints in an oddball frequency-sweep design for visual discrimination of complex images (face exemplars). Sixteen participants viewed sequences of ascending presentation durations, from 25 to 333 ms (40–3 Hz stimulation rate) while their electroencephalogram (EEG) was recorded. Throughout each sequence, the same unfamiliar face picture was repeated with variable size and luminance changes while different unfamiliar facial identities appeared every 1 s (1 Hz). A neural face individuation response, tagged at 1 Hz and its unique harmonics, emerged over the occipito-temporal cortex at 50 ms stimulus duration (25–100 ms across individuals), with an optimal response reached at 170 ms stimulus duration. In a subsequent experiment, identity changes appeared non-periodically within fixed-frequency sequences while the same participants performed an explicit face individuation task. The behavioral face individuation response also emerged at 50 ms presentation time, and behavioral accuracy correlated with individual participants’ neural response amplitude in a weighted middle stimulus duration range (50–125 ms). Moreover, the latency of the neural response peaking between 180 and 200 ms correlated strongly with individuals’ behavioral accuracy in this middle duration range, as measured independently. These observations point to the minimal (50 ms) and optimal (170 ms) stimulus durations for human face individuation and provide novel evidence that inter-individual differences in the magnitude and latency of early, high-level neural responses are predictive of behavioral differences in performance at this function. [less ▲]

Harmonic amplitude summation for frequency-tagging analysis

in Journal of Cognitive Neuroscience (2021)

In the approach of frequency tagging, stimuli that are presented periodically generate periodic responses of the brain. Following a transformation into the frequency domain, the brain’s response is often ... [more ▼]

In the approach of frequency tagging, stimuli that are presented periodically generate periodic responses of the brain. Following a transformation into the frequency domain, the brain’s response is often evident at the frequency of stimulation, F, and its higher harmonics (2F, 3F, etc.). This approach is increasingly used in neuroscience, as it affords objective measures to characterize brain function. However, whether these specific harmonic frequency responses should be combined for analysis, and if so, how, remains an outstanding issue. In most studies, higher harmonic responses have not been described or were described only individually; in other studies, harmonics have been combined with various approaches, e.g., averaging and root mean squared summation. A rationale for these approaches in the context of frequency-based analysis principles, and understanding of how they relate to the brain’s response amplitudes in the time domain, has been missing. Here, with these elements addressed, the summation of (baseline-corrected) harmonic amplitude is recommended. [less ▲]

Understanding human individuation of unfamiliar faces with oddball fast periodic visual stimulation and electroencephalography

in European Journal of Neuroscience (2020)

To investigate face individuation (FI), a critical brain function in the human species, an oddball fast periodic visual stimulation (FPVS) approach was recently introduced (Liu‐Shuang et al ... [more ▼]

To investigate face individuation (FI), a critical brain function in the human species, an oddball fast periodic visual stimulation (FPVS) approach was recently introduced (Liu‐Shuang et al., Neuropsychologia, 2014, 52, 57). In this paradigm, an image of an unfamiliar “base” facial identity is repeated at a rapid rate F (e.g., 6 Hz) and different unfamiliar “oddball” facial identities are inserted every nth item, at a F/n rate (e.g., every 5th item, 1.2 Hz). This stimulation elicits FI responses at F/n and its harmonics (2F/n, 3F/n, etc.), reflecting neural discrimination between oddball versus base facial identities, which is quantified in the frequency domain of the electroencephalogram (EEG). This paradigm, used in 20 published studies, demonstrates substantial advantages for measuring FI in terms of validity, objectivity, reliability, and sensitivity. Human intracerebral recordings suggest that this FI response originates from neural populations in the lateral inferior occipital and fusiform gyri, with a right hemispheric dominance consistent with the localization of brain lesions specifically affecting facial identity recognition (prosopagnosia). Here, we summarize the contributions of the oddball FPVS framework toward understanding FI, including its (a)typical development, with early studies supporting the application of this technique to clinical testing (e.g., autism spectrum disorder). This review also includes an in‐depth analysis of the paradigm's methodology, with guidelines for designing future studies. A large‐scale group analysis compiling data across 130 observers provides insights into the oddball FPVS FI response properties. Overall, we recommend the oddball FPVS paradigm as an alternative approach to behavioral or traditional event‐related potential EEG measures of face individuation. [less ▲]

All-or-none face categorization in the human brain

in NeuroImage (2020)

Visual categorization is integral for our interaction with the natural environment. In this process, similar selective responses are produced to a class of variable visual inputs. Whether categorization ... [more ▼]

Visual categorization is integral for our interaction with the natural environment. In this process, similar selective responses are produced to a class of variable visual inputs. Whether categorization is supported by partial (graded) or absolute (all-or-none) neural responses in high-level human brain regions is largely unknown. We address this issue with a novel frequency-sweep paradigm probing the evolution of face categorization responses between the minimal and optimal stimulus presentation times. In a first experiment, natural images of variable non-face objects were progressively swept from 120 to 3 ​Hz (8.33–333 ​ms duration) in rapid serial visual presentation sequences. Widely variable face exemplars appeared every 1 ​s, enabling an implicit frequency-tagged face-categorization electroencephalographic (EEG) response at 1 ​Hz. Face-categorization activity emerged with stimulus durations as brief as 17 ​ms (17–83 ​ms across individual participants) but was significant with 33 ​ms durations at the group level. The face categorization response amplitude increased until 83 ​ms stimulus duration (12 ​Hz), implying graded categorization responses. In a second EEG experiment, faces appeared non-periodically throughout such sequences at fixed presentation rates, while participants explicitly categorized faces. A strong correlation between response amplitude and behavioral accuracy across frequency rates suggested that dilution from missed categorizations, rather than a decreased response to each face stimulus, accounted for the graded categorization responses as found in Experiment 1. This was supported by (1) the absence of neural responses to faces that participants failed to categorize explicitly in Experiment 2 and (2) equivalent amplitudes and spatio-temporal signatures of neural responses to behaviorally categorized faces across presentation rates. Overall, these observations provide original evidence that high-level visual categorization of faces, starting at about 100 ​ms following stimulus onset in the human brain, is variable across observers tested under tight temporal constraints, but occurs in an all-or-none fashion. [less ▲]