Timothy D. Sweeny

Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles

Stressful social conditions, such as isolation, that occur during sensitive developmental periods may alter present and future social behavior. Changes in the neuroendocrine mechanisms closely associated with affiliative behaviors and stress reactivity are likely to underlie these changes in behavior. In the present study, we assessed the effects of post-weaning social housing conditions on the neuropeptides arginine vasopressin (AVP) and oxytocin (OT), and components of the hypothalamic-pituitary-adrenal axis (corticotropin releasing factor: [CRF], and corticosterone: [CORT]) in the prairie vole (Microtus ochrogaster), a socially monogamous bi-parental rodent. Following weaning at 21 days of age, prairie voles were maintained in one of three housing conditions: social isolation (isolate), paired with a same sex sibling (sibling) or paired with a stranger (stranger) of the same sex and age. Housing conditions were maintained for either 4 or 21 days. Central CRF, AVP and OT immunoreactivity (ir) were quantified and circulating plasma CORT, AVP and OT were assayed. Isolated voles had higher CRF-ir in the paraventricular nucleus of the hypothalamus (PVN) compared with sibling and stranger housed voles. Plasma CORT was significantly higher in isolates. AVP-ir was significantly lower in the PVN of isolate females compared to either sibling females or stranger females. However, AVP-ir was significantly higher in the supraoptic nucleus (SON) of isolates compared to siblings. There were no differences in central OT-ir or plasma OT. These results identify neuroendocrine mechanisms which respond to isolation and potentially modulate behavior.

Perceiving group behavior: sensitive ensemble coding mechanisms for biological motion of human crowds.

Many species, including humans, display group behavior. Thus, perceiving crowds may be important for social interaction and survival. Here, we provide the first evidence that humans use ensemble-coding mechanisms to perceive the behavior of a crowd of people with surprisingly high sensitivity. Observers estimated the headings of briefly presented crowds of point-light walkers that differed in the number and headings of their members (i.e., people in differently sized crowds had identical or increasingly variable directions of walking). We found that observers rapidly pooled information from multiple walkers to estimate the heading of a crowd. This ensemble code was precise; observers perceived the behavior of a crowd better than the behavior of an individual. We also showed that this pooling provided tolerance against crowd variability and may cause a chaotic group to cohere into a unified Gestalt. Sensitive perception of a crowds behavior required integration of human form and motion, suggesting that the ensemble code was generated in high-level visual areas. Overall, these mechanisms may reflect the prevalence of crowd behavior in nature and a social benefit for perceiving crowds as unified entities.

Long-lasting effects of subliminal affective priming from facial expressions

Unconscious processing of stimuli with emotional content can bias affective judgments. Is this subliminal affective priming merely a transient phenomenon manifested in fleeting perceptual changes, or are long-lasting effects also induced? To address this question, we investigated memory for surprise faces 24 h after they had been shown with 30-ms fearful, happy, or neutral faces. Surprise faces subliminally primed by happy faces were initially rated as more positive, and were later remembered better, than those primed by fearful or neutral faces. Participants likely to have processed primes supraliminally did not respond differentially as a function of expression. These results converge with findings showing memory advantages with happy expressions, though here the expressions were displayed on the face of a different person, perceived subliminally, and not present at test. We conclude that behavioral biases induced by masked emotional expressions are not ephemeral, but rather can last at least 24 h.

Perceiving Crowd Attention Ensemble Perception of a Crowd’s Gaze

In nearly every interpersonal encounter, people readily gather socio-visual cues to guide their behavior. Intriguingly, social information is most effective in directing behavior when it is perceived in crowds. For example, the shared gaze of a crowd is more likely to direct attention than is a single person’s gaze. Are people equipped with mechanisms to perceive a crowd’s gaze as an ensemble? Here, we provide the first evidence that the visual system extracts a summary representation of a crowd’s attention; observers rapidly pooled information from multiple crowd members to perceive the direction of a group’s collective gaze. This pooling occurred in high-level stages of visual processing, with gaze perceived as a global-level combination of information from head and pupil rotation. These findings reveal an important and efficient mechanism for assessing crowd gaze, which could underlie the ability to perceive group intentions, orchestrate joint attention, and guide behavior.

Humans Use Summary Statistics to Perceive Auditory Sequences

In vision, humans use summary statistics (e.g., the average facial expression of a crowd) to efficiently perceive the gist of groups of features. Here, we present direct evidence that ensemble coding is also important for auditory processing. We found that listeners could accurately estimate the mean frequency of a set of logarithmically spaced pure tones presented in a temporal sequence (Experiment 1). Their performance was severely reduced when only a subset of tones from a given sequence was presented (Experiment 2), which demonstrates that ensemble coding is based on a substantial number of the tones in a sequence. This precise ensemble coding occurred despite very limited representation of individual tones from the sequence: Listeners were poor at identifying specific individual member tones (Experiment 3) and at determining their positions in the sequence (Experiment 4). Together, these results indicate that summary statistical coding is not limited to visual processing and is an important auditory mechanism for extracting ensemble frequency information from sequences of sounds.

Reference repulsion in the categorical perception of biological motion.

Perceiving biological motion is important for understanding the intentions and future actions of others. Perceiving an approaching persons behavior may be particularly important, because such behavior often precedes social interaction. To this end, the visual system may devote extra resources for perceiving an oncoming persons heading. If this were true, humans should show increased sensitivity for perceiving approaching headings, and as a result, a repulsive perceptual effect around the categorical boundary of leftward/rightward motion. We tested these predictions and found evidence for both. First, observers were especially sensitive to the heading of an approaching person; variability in estimates of a persons heading decreased near the category boundary of leftward/rightward motion. Second, we found a repulsion effect around the category boundary; a person walking approximately toward the observer was perceived as being repelled away from straight ahead. This repulsive effect was greatly exaggerated for perception of a very briefly presented person or perception of a chaotic crowd, suggesting that repulsion may protect against categorical errors when sensory noise is high. The repulsion effect with a crowd required integration of local motion and human form, suggesting an origin in high-level stages of visual processing. Similar repulsive effects may underlie categorical perception with other social features. Overall, our results show that a persons direction of walking is categorically perceived, with improved sensitivity at the category boundary and a concomitant repulsion effect.

Sounds exaggerate visual shape

While perceiving speech, people see mouth shapes that are systematically associated with sounds. In particular, a vertically stretched mouth produces a /woo/ sound, whereas a horizontally stretched mouth produces a /wee/ sound. We demonstrate that hearing these speech sounds alters how we see aspect ratio, a basic visual feature that contributes to perception of 3D space, objects and faces. Hearing a /woo/ sound increases the apparent vertical elongation of a shape, whereas hearing a /wee/ sound increases the apparent horizontal elongation. We further demonstrate that these sounds influence aspect ratio coding. Viewing and adapting to a tall (or flat) shape makes a subsequently presented symmetric shape appear flat (or tall). These aspect ratio aftereffects are enhanced when associated speech sounds are presented during the adaptation period, suggesting that the sounds influence visual population coding of aspect ratio. Taken together, these results extend previous demonstrations that visual information constrains auditory perception by showing the converse - speech sounds influence visual perception of a basic geometric feature.

Awareness Becomes Necessary Between Adaptive Pattern Coding of Open and Closed Curvatures

Visual pattern processing becomes increasingly complex along the ventral pathway, from the low-level coding of local orientation in the primary visual cortex to the high-level coding of face identity in temporal visual areas. Previous research using pattern aftereffects as a psychophysical tool to measure activation of adaptive feature coding has suggested that awareness is relatively unimportant for the coding of orientation, but awareness is crucial for the coding of face identity. We investigated where along the ventral visual pathway awareness becomes crucial for pattern coding. Monoptic masking, which interferes with neural spiking activity in low-level processing while preserving awareness of the adaptor, eliminated open-curvature aftereffects but preserved closed-curvature aftereffects. In contrast, dichoptic masking, which spares spiking activity in low-level processing while wiping out awareness, preserved open-curvature aftereffects but eliminated closed-curvature aftereffects. This double dissociation suggests that adaptive coding of open and closed curvatures straddles the divide between weakly and strongly awareness-dependent pattern coding.

Simultaneous shape repulsion and global assimilation in the perception of aspect ratio

Although local interactions involving orientation and spatial frequency are well understood, less is known about spatial interactions involving higher level pattern features. We examined interactive coding of aspect ratio, a prevalent two-dimensional feature. We measured perception of two simultaneously flashed ellipses by randomly post-cueing one of them and having observers indicate its aspect ratio. Aspect ratios interacted in two ways. One manifested as an aspect-ratio-repulsion effect. For example, when a slightly tall ellipse and a taller ellipse were simultaneously flashed, the less tall ellipse appeared flatter and the taller ellipse appeared even taller. This repulsive interaction was long range, occurring even when the ellipses were presented in different visual hemifields. The other interaction manifested as a global assimilation effect. An ellipse appeared taller when it was a part of a global vertical organization than when it was a part of a global horizontal organization. The repulsion and assimilation effects temporally dissociated as the former slightly strengthened, and the latter disappeared when the ellipse-to-mask stimulus onset asynchrony was increased from 40 to 140 ms. These results are consistent with the idea that shape perception emerges from rapid lateral and hierarchical neural interactions.

Internal curvature signal and noise in low- and high-level vision

How does internal processing contribute to visual pattern perception? By modeling visual search performance, we estimated internal signal and noise relevant to perception of curvature, a basic feature important for encoding of three-dimensional surfaces and objects. We used isolated, sparse, crowded, and face contexts to determine how internal curvature signal and noise depended on image crowding, lateral feature interactions, and level of pattern processing. Observers reported the curvature of a briefly flashed segment, which was presented alone (without lateral interaction) or among multiple straight segments (with lateral interaction). Each segment was presented with no context (engaging low-to-intermediate-level curvature processing), embedded within a face context as the mouth (engaging high-level face processing), or embedded within an inverted-scrambled-face context as a control for crowding. Using a simple, biologically plausible model of curvature perception, we estimated internal curvature signal and noise as the mean and standard deviation, respectively, of the Gaussian-distributed population activity of local curvature-tuned channels that best simulated behavioral curvature responses. Internal noise was increased by crowding but not by face context (irrespective of lateral interactions), suggesting prevention of noise accumulation in high-level pattern processing. In contrast, internal curvature signal was unaffected by crowding but modulated by lateral interactions. Lateral interactions (with straight segments) increased curvature signal when no contextual elements were added, but equivalent interactions reduced curvature signal when each segment was presented within a face. These opposing effects of lateral interactions are consistent with the phenomena of local-feature contrast in low-level processing and global-feature averaging in high-level processing.