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Odor-driven face-like categorization in the human infant brain.

ABSTRACT: Understanding how the young infant brain starts to categorize the flurry of ambiguous sensory inputs coming in from its complex environment is of primary scientific interest. Here, we test the hypothesis that senses other than vision play a key role in initiating complex visual categorizations in 20 4-mo-old infants exposed either to a baseline odor or to their mother's odor while their electroencephalogram (EEG) is recorded. Various natural images of objects are presented at a 6-Hz rate (six images/second), with face-like object configurations of the same object categories (i.e., eliciting face pareidolia in adults) interleaved every sixth stimulus (i.e., 1 Hz). In the baseline odor context, a weak neural categorization response to face-like stimuli appears at 1 Hz in the EEG frequency spectrum over bilateral occipitotemporal regions. Critically, this face-like-selective response is magnified and becomes right lateralized in the presence of maternal body odor. This reveals that nonvisual cues systematically associated with human faces in the infant's experience shape the interpretation of face-like configurations as faces in the right hemisphere, dominant for face categorization. At the individual level, this intersensory influence is particularly effective when there is no trace of face-like categorization in the baseline odor context. These observations provide evidence for the early tuning of face-(like)-selective activity from multisensory inputs in the developing brain, suggesting that perceptual development integrates information across the senses for efficient category acquisition, with early maturing systems such as olfaction driving the acquisition of categories in later-developing systems such as vision.

SUBMITTER: Rekow D

PROVIDER: S-EPMC8166123 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

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Odor-driven face-like categorization in the human infant brain.

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