Culture differences in neural processing of faces and houses in the ventral visual cortex.

Behavioral and eye-tracking studies on cultural differences have found that while Westerners have a bias for analytic processing and attend more to face features, East Asians are more holistic and attend more to contextual scenes. In this neuroimaging study, we hypothesized that these culturally different visual processing styles would be associated with cultural differences in the selective activity of the fusiform regions for faces, and the parahippocampal and lingual regions for contextual stimuli. East Asians and Westerners passively viewed face and house stimuli during an functional magnetic resonance imaging experiment. As expected, we observed more selectivity for faces in Westerners in the left fusiform face area (FFA) reflecting a more analytic processing style. Additionally, Westerners showed bilateral activity to faces in the FFA whereas East Asians showed more right lateralization. In contrast, no cultural differences were detected in the parahippocampal place area (PPA), although there was a trend for East Asians to show greater house selectivity than Westerners in the lingual landmark area, consistent with more holistic processing in East Asians. These findings demonstrate group biases in Westerners and East Asians that operate on perceptual processing in the brain and are consistent with previous eye-tracking data that show cultural biases to faces.

Sleep deprivation impairs object-selective attention: a view from the ventral visual cortex.

BACKGROUND: Most prior studies on selective attention in the setting of total sleep deprivation (SD) have focused on behavior or activation within fronto-parietal cognitive control areas. Here, we evaluated the effects of SD on the top-down biasing of activation of ventral visual cortex and on functional connectivity between cognitive control and other brain regions. METHODOLOGY/PRINCIPAL FINDINGS: Twenty-three healthy young adult volunteers underwent fMRI after a normal night of sleep (RW) and after sleep deprivation in a counterbalanced manner while performing a selective attention task. During this task, pictures of houses or faces were randomly interleaved among scrambled images. Across different blocks, volunteers responded to house but not face pictures, face but not house pictures, or passively viewed pictures without responding. The appearance of task-relevant pictures was unpredictable in this paradigm. SD resulted in less accurate detection of target pictures without affecting the mean false alarm rate or response time. In addition to a reduction of fronto-parietal activation, attending to houses strongly modulated parahippocampal place area (PPA) activation during RW, but this attention-driven biasing of PPA activation was abolished following SD. Additionally, SD resulted in a significant decrement in functional connectivity between the PPA and two cognitive control areas, the left intraparietal sulcus and the left inferior frontal lobe. CONCLUSIONS/SIGNIFICANCE: SD impairs selective attention as evidenced by reduced selectivity in PPA activation. Further, reduction in fronto-parietal and ventral visual task-related activation suggests that it also affects sustained attention. Reductions in functional connectivity may be an important additional imaging parameter to consider in characterizing the effects of sleep deprivation on cognition.

Lapsing when sleep deprived: neural activation characteristics of resistant and vulnerable individuals.

Lapses of attention, in the form of delayed responses to salient stimuli, increase in frequency for some but not all persons after sleep deprivation (SD). To identify patterns of task-related brain activation that might explain differences in vulnerability to SD, we performed fMRI on participants during a visual, selective attention task. We analyzed the correct responses in a trial-by-trial fashion to model the effects of response time. Stimulus contrast was varied to modulate perceptual difficulty. Attentional lapses and low-contrast stimuli were independently associated with increased signal in fronto-parietal regions associated with biasing attention. Sleep-deprived vulnerable individuals showed reduced top down fronto-parietal signal across all levels of image contrast and this reduction was particularly significant during lapses. There was concurrent reduction in extrastriate cortex and thalamus activation. Non-vulnerable persons showed a trend towards higher top-down biasing of attention and preserved visual cortex activation during SD lapses. A major contributor to performance degradation in SD appears to be a reduction in top-down biasing of attention that is independent of task difficulty.

Sleep deprivation and its effects on object-selective attention.

Sleep deprivation (SD) affects attention but it is an open question as to whether all subtypes of attention are similarly affected. We investigated the effects of 24 h of total SD on object-selective attention. 26 healthy, young adults viewed quartets of alternating faces or place scenes and performed selective judgments on faces only, scenes only or both faces and scenes. Volunteers underwent fMRI following a normal night of sleep and again following approximately 24 h of total sleep deprivation in a counterbalanced fashion. Sleep deprivation resulted in slower and less accurate picture classification as well as poorer recognition memory for scenes. Attention strongly modulated activation in the Parahippocampal Place Area (PPA). Task-related activation in the fronto-parietal cortex and PPA was reduced in SD, but the relative modulation of PPA activation by attention was preserved. Psychophysiological interaction between the left intra-parietal sulcus and the PPA that was clearly present after a normal night of sleep was reduced below threshold following SD suggesting that PPI may be a more sensitive method of detecting change in selective attention. Sleep deprivation may affect object-selective attention in addition to exerting a task-independent deficit in attention.

Culture modulates eye-movements to visual novelty.

BACKGROUND: When viewing complex scenes, East Asians attend more to contexts whereas Westerners attend more to objects, reflecting cultural differences in holistic and analytic visual processing styles respectively. This eye-tracking study investigated more specific mechanisms and the robustness of these cultural biases in visual processing when salient changes in the objects and backgrounds occur in complex pictures. METHODOLOGY/PRINCIPAL FINDINGS: Chinese Singaporean (East Asian) and Caucasian US (Western) participants passively viewed pictures containing selectively changing objects and background scenes that strongly captured participants' attention in a data-driven manner. We found that although participants from both groups responded to object changes in the pictures, there was still evidence for cultural divergence in eye-movements. The number of object fixations in the US participants was more affected by object change than in the Singapore participants. Additionally, despite the picture manipulations, US participants consistently maintained longer durations for both object and background fixations, with eye-movements that generally remained within the focal objects. In contrast, Singapore participants had shorter fixation durations with eye-movements that alternated more between objects and backgrounds. CONCLUSIONS/SIGNIFICANCE: The results demonstrate a robust cultural bias in visual processing even when external stimuli draw attention in an opposite manner to the cultural bias. These findings also extend previous studies by revealing more specific, but consistent, effects of culture on the different aspects of visual attention as measured by fixation duration, number of fixations, and saccades between objects and backgrounds.

Donepezil improves episodic memory in young individuals vulnerable to the effects of sleep deprivation.

STUDY OBJECTIVES: We investigated if donepezil, a long-acting orally administered cholinesterase inhibitor, would reduce episodic memory deficits associated with 24 h of sleep deprivation. DESIGN: Double-blind, placebo-controlled, crossover study involving 7 laboratory visits over 2 months. Participants underwent 4 functional MRI scans; 2 sessions (donepezil or placebo) followed a normal night's sleep, and 2 sessions followed a night of sleep deprivation. SETTING: The study took place in a research laboratory. PARTICIPANTS: 26 young, healthy volunteers with no history of any sleep, psychiatric, or neurologic disorders. INTERVENTIONS: 5 mg of donepezil was taken once daily for approximately 17 days. MEASUREMENTS AND RESULTS: Subjects were scanned while performing a semantic judgment task and tested for word recognition outside the scanner 45 minutes later. Sleep deprivation increased the frequency of non-responses at encoding and impaired delayed recognition. No benefit of donepezil was evident when participants were well rested. When sleep deprived, individuals who showed greater performance decline improved with donepezil, whereas more resistant individuals did not benefit. Accompanying these behavioral effects, there was corresponding modulation of task-related activation in functionally relevant brain regions. Brain regions identified in relation to donepezil-induced alteration in non-response rates could be distinguished from regions relating to improved recognition memory. This suggests that donepezil can improve delayed recognition in sleep-deprived persons by improving attention as well as enhancing memory encoding. CONCLUSIONS: Donepezil reduced decline in recognition performance in individuals vulnerable to the effects of sleep deprivation. Additionally, our findings demonstrate the utility of combined fMRI-behavior evaluation in psychopharmacological studies.

Lapsing during sleep deprivation is associated with distributed changes in brain activation.

Lapses of attention manifest as delayed behavioral responses to salient stimuli. Although they can occur even after a normal night's sleep, they are longer in duration and more frequent after sleep deprivation (SD). To identify changes in task-associated brain activation associated with lapses during SD, we performed functional magnetic resonance imaging during a visual, selective attention task and analyzed the correct responses in a trial-by-trial manner modeling the effects of response time. Separately, we compared the fastest 10% and slowest 10% of correct responses in each state. Both analyses concurred in finding that SD-related lapses differ from lapses of equivalent duration after a normal night's sleep by (1) reduced ability of frontal and parietal control regions to raise activation in response to lapses, (2) dramatically reduced visual sensory cortex activation, and (3) reduced thalamic activation during lapses that contrasted with elevated thalamic activation during nonlapse periods. Despite these differences, the fastest responses after normal sleep and after SD elicited comparable frontoparietal activation, suggesting that performing a task while sleep deprived involves periods of apparently normal neural activation interleaved with periods of depressed cognitive control, visual perceptual functions, and arousal. These findings reveal for the first time some of the neural consequences of the interaction between efforts to maintain wakefulness and processes that initiate involuntary sleep in sleep-deprived persons.

Inter-relationships between attention, activation, fMR adaptation and long-term memory.

fMR adaptation in the ventral visual pathway reflects information processing that may contribute to implicit and explicit memory. In experiments that employed <1 s repetition lag, we found that attention increases adaptation for repeated objects in brain regions at the top of the visual processing hierarchy (anterior fusiform and parahippocampal gyri) but that it can still appear with minimal attention in most of the fusiform bilaterally. Of the ventral visual regions showing adaptation, the parahippocampal region and LOC showed the strongest correlation between adaptation magnitude and recognition memory across subjects. Although there was some overlap, regions showing correlations between adaptation and priming lay more posteriorly within the fusiform region. The positive association between encoding-related activation and adaptation suggests that over an entire test set, memory performance can be determined by neural events occurring in the peristimulus period. This may reflect stronger engagement of attention at encoding.

Age and culture modulate object processing and object-scene binding in the ventral visual area.

Behavioral differences in the visual processing of objects and backgrounds as a function of cultural group are well documented. Recent neuroimaging evidence also points to cultural differences in neural activation patterns. Compared with East Asians, Westerners' visual processing is more object focused, and they activate neural structures that reflect this bias for objects. In a recent adaptation study, East Asian older adults showed an absence of an object-processing area but normal adaptation for background areas. In the present study, 75 young and old adults (half East Asian and half Western) were tested in an fMR-adaptation study to examine differences in object and background processing as well as object-background binding. We found equivalent background processing in the parahippocampal gyrus in all four groups, diminished binding processes in the hippocampus in elderly East Asians and Westerners, and diminished object processing in elderly versus young adults in the lateral occipital complex. Moreover, elderly East Asians showed significantly less adaptation response in the object areas than did elderly Westerners. These findings demonstrate the malleability of perceptual processes as a result of differences in cohort-specific experiences or in cultural exposure over time.

Contextual interference in recognition memory with age.

Previous behavioral research suggests that although elderly adults' memory benefits from supportive context, misleading or irrelevant contexts produce greater interference. In the present study, we use event-related fMRI to investigate age differences when processing contextual information to make recognition judgments. Twenty-one young and twenty elderly incidentally encoded pictures of objects presented in meaningful contexts, and completed a memory test for the objects presented in identical or novel contexts. Elderly committed more false alarms than young when novel objects were presented in familiar, but task-irrelevant, contexts. Elderly showed reduced engagement of bilateral dorsolateral prefrontal cortex and anterior cingulate relative to young, reflecting disruption of a cognitive control network for processing context with age. Disruption occurred for both high and low-performing elderly, suggesting that cognitive control deficits are pervasive with age. Despite showing disruption of the cognitive control network, high-performing elderly recruited additional middle and medial frontal regions that were not recruited by either low-performing elderly or young adults. This suggests that high-performing elderly may compensate for the disruption of the cognitive control network by recruiting additional frontal resources to overcome cognitive control deficits that affect recognition memory.

Age-related changes in object processing and contextual binding revealed using fMR adaptation.

Using fMR adaptation, we studied the effects of aging on the neural processing of passively viewed naturalistic pictures composed of a prominent object against a background scene. Spatially distinct neural regions showing specific patterns of adaptation to objects, background scenes, and contextual integration (binding) were identified in young adults. Older adults did not show adaptation responses corresponding to binding in the medial-temporal areas. They also showed an adaptation deficit for objects whereby their lateral occipital complex (LOC) did not adapt to repeated objects in the context of a changing background. The LOC could be activated, however, when objects were presented without a background. Moreover, the adaptation deficit for objects viewed against backgrounds was reversed when elderly subjects were asked to attend to objects while viewing these complex pictures. These findings suggest that the elderly have difficulty with simultaneous processing of objects and backgrounds that, in turn, could contribute to deficient contextual binding.